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临床研究
T1-mapping技术对肿瘤坏死因子-α拮抗剂治疗中轴型脊柱关节病疗效监测的初步研究
俞顺 苏家威 林敏贵 陈贤源 马明平

Cite this article as: Yu S, Su JW, Lin MG, et al. A preliminary study on the efficacy of tumor necrosis factor alpha antagonists in the treatment of axial spondyloarthropathy by T1-mapping technique[J]. Chin J Magn Reson Imaging, 2022, 13(1): 21-25, 36.本文引用格式:俞顺, 苏家威, 林敏贵, 等. T1-mapping技术对肿瘤坏死因子-α拮抗剂治疗中轴型脊柱关节病疗效监测的初步研究[J]. 磁共振成像, 2022, 13(1): 21-25, 36. DOI:10.12015/issn.1674-8034.2022.01.005.


[摘要] 目的 探讨运用T1-mapping技术监测肿瘤坏死因子-α (tumor necrosis factor-α,TNF-α)拮抗剂(TNFi)治疗中轴型脊柱关节病(axial spondyloarthropathy,axSpA)疗效,以期对axSpA炎症活动性和疗效监测提供有效的量化指标。材料与方法 纳入114例研究对象,对照组15例,病例组99例,病例组中20例患者经过系统的TNFi治疗为治疗组。病例组分为活动组和非活动组,活动组分为中度活动组、活动度提高组、活动度非常高组三个亚组,治疗组根据治疗的不同周期分为治疗前组、治疗3周组、治疗6周组和治疗12周组。所有对象均行T1-mapping序列检查,比较对照组、病例组以及病例组各亚组之间骶髂关节软骨下骨髓区域T1-mapping值的差异,运用ROC曲线分析诊断效能,并根据治疗组不同治疗周期T1-mapping值下降率对疗效进行监测。结果 (1)各组骶髂关节骶侧、髂侧关节软骨下骨髓区域T1-mapping值差异均无统计学意义,P>0.05;(2)与对照组相比,病例组骶髂关节软骨下骨髓区域T1-mapping值表现为不同程度的上升,T1-mapping值的差异对活动度提高组和活动度非常高组具有很好的诊断效能;(3)治疗组中不同治疗周期骶髂关节软骨下骨髓区域T1-mapping值的下降率能够有效监测疗效。结论 T1-mapping技术可以量化评估axSpA炎症活动性,并有效监测疗效,有益于临床个体化治疗、及时调整治疗方案。
[Abstract] Objective To explore the use of MRI T1-mapping technique to evaluate the efficacy of tumor necrosis factor-α antagonists in the treatment of axial spondyloarthropathy (axSpA), in order to provide effective quantitative indicators for the evaluation of axSpA treatment.Materials and Methods One hundred and fourteen study subjects were included, of which 15 normal sacroiliac joint subjects excluded from the diagnosis of axSpA were the control group, and 99 clinically confirmed axSpA patients were the case group, twenty patients in the case group were treated with systemic TNF-α antagonists as the treatment group. The case group was divided into active group and inactive group. The active group was divided into three subgroups: moderate activity group, high activity group and very high activity group. The treatment group was divided into pre-treatment group and 3 weeks treatment group, 6 weeks treatment group and 12 weeks treatment group according to the different time of treatment. All subjects underwent T1-mapping sequence examination to compare the differences in T1-mapping values of the sacroiliac joint subchondral bone marrow area between the control group, the case group, and the subgroups of the case group, using ROC curve to analyze the diagnostic efficacy and monitoring of therapeutic efficacy of different treatment cycles in the treatment group.Results (1) There was no significant difference in the T1-mapping value of the subchondral bone marrow area of the sacroiliac joint and iliac joint in each group, all P>0.05; (2) Compared with the control group, the T1-mapping value of the bone marrow area under the sacroiliac articular cartilage of the case group increased to varying degrees, T1-mapping value had a good diagnostic efficiency for the high activity group and the very high activity group; (3) The decrease rate of T1-mapping value in the subchondral bone marrow area of sacroiliac joint in different treatment cycles in the treatment group could effectively monitor the curative effect.Conclusions T1-mapping technology can quantitatively evaluate axSpA inflammatory activity, and effectively monitor the efficacy, which is beneficial to clinical individualized treatment and timely adjustment of treatment plans.
[关键词] 中轴型脊柱关节病;强直性脊柱炎;肿瘤坏死因子-α;T1-mapping;骨髓水肿
[Keywords] axial spondyloarthropathy;ankylosing spondylitis;tumor necrosis factor-α;T1-mapping;bone marrow edema

俞顺 *   苏家威    林敏贵    陈贤源    马明平   

福建医科大学省立临床医学院 福建省立医院放射科,福州 350001

俞顺,E-mail:76429310@qq.com

全部作者均声明无利益冲突。


基金项目: 福建省自然科学基金项目计划 2017J01172 中华国际医学交流基金会SKY影像科研基金发展项目 Z-2014-07-1912-14 福建省卫生健康中青年骨干人才培养项目 2020GGA005
收稿日期:2021-06-21
接受日期:2021-11-10
中图分类号:R445.2  R681.5 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2022.01.005
本文引用格式:俞顺, 苏家威, 林敏贵, 等. T1-mapping技术对肿瘤坏死因子-α拮抗剂治疗中轴型脊柱关节病疗效监测的初步研究[J]. 磁共振成像, 2022, 13(1): 21-25, 36. DOI:10.12015/issn.1674-8034.2022.01.005

       中轴型脊柱关节病(axial spondyloarthropathy, axSpA)是一种以炎性腰背痛为主要特征表现的慢性自身免疫性疾病,我国发病率约0.2%~0.54%[1],青年男性多见,起病隐匿,病程持续,病情反复,若持续进展,最终导致脊柱(关节)骨性强直,极大影响患者的生活质量和劳动能力,是较严重的公共卫生问题。早诊断、早治疗是争取良好预后和改善生活质量的关键[2]。目前临床上对axSpA患者治疗后监测多用强直性脊柱炎病情活动度评分(ankylosing spondylitis disease activity score,ASDAS)[3],以数个基于患者的主观评价问题为基础的ASDAS评分,难以准确反映出疾病本身的活动状态。肿瘤坏死因子-α (tumor necrosis factor-α,TNF-α)抑制剂(TNFi)作为活动期axSpA患者的一线用药,疗效已得到广泛肯定[4, 5, 6],但如何监测患者用药后炎症活动状态并调整治疗方案,仍是临床上亟待解决的问题。MRI T1-mapping技术不仅兼顾了常规MRI无辐射、较好的软组织分辨等特点,且可以检测组织中水分子、蛋白多糖、胶原含量等的微小变化,并通过T1-mapping值体现,有望成为骨关节病变早期诊断及病情监测的敏感指标[7, 8]。本研究拟运用MRI T1-mapping技术量化评估axSpA骶髂关节软骨下骨髓水肿程度,以期对axSpA炎症活动性和疗效监测提供有效的定量指标。

1 材料与方法

1.1 一般资料及病例分组

       回顾性收集2017年10月至2020年5月福建省立医院风湿科收治的99例axSpA患者病例为病例组,15例排除axSpA诊断的正常骶髂关节受检者为对照组,病例组中选择经过系统的TNFi治疗的20例为治疗组。病例组纳入标准:(1)符合国际axSpA评价工作组(Assessment of Spondyloarthritis International Society,ASAS)推出的2009年axSpA分类标准[9];(2)腰背疼痛持续1年以上,根据修订版纽约标准确诊为AS;(3)临床及MRI检查资料齐全。对照组纳入标准:(1)单纯的慢性下腰痛,均行骶髂关节MRI检查;(2)短TI反转恢复(short TI inversion recovery,STIR)序列双侧骶髂关节骨质未见高信号,且排除axSpA诊断。两组排除标准一致:原发性骨质疏松,免疫系统疾病,肿瘤,合并其他骨病或近6个月有激素和免疫药物用药史。经过福建省立医院风湿科系统的TNFi (依那西普,每周一次,每次50 mg)治疗的患者为治疗组,治疗组在治疗前组、治疗3周、治疗6周和治疗12周均进行一次相应的骶髂关节磁共振检查,治疗前磁共振检查在治疗开始前7天内完成。

       对照组15例中男9例,女6例,年龄17~59 (35.6±13.8)岁。病例组99例中根据ASDAS评分[3]分为活动组(ASDAS≥1.3) 79例、非活动组(ASDAS<1.3) 20例。活动组中男53例,女26例,年龄14~71 (36.1±14.3)岁;非活动组中男7例,女13例,年龄17~54 (33.2±10.6)岁。活动组79例再根据ASDAS评分分为中度活动组(1.3≤ASDAS<2.1) 18例、活动度提高组(2.1≤ASDAS≤3.5) 42例、活动度非常高组(ASDAS>3.5) 19例3个亚组。治疗组20例中男11例、女9例、年龄17~54 (28.5±9.9)岁。对照组、病例组、活动组3个亚组以及治疗组组间的患者性别(P=0.946)、年龄(P=0.949)比较,差异均无统计学意义,具有可比性。本研究经医院伦理委员会批准(批准文号:K2016-09-023,K2018-03-008),所有患者签署知情同意书且全程参与研究。

1.2 检查方法

       本组114例均行MRI扫描,采用Siemens Aera 1.5 T磁共振扫描仪,患者仰卧位头先进,行横轴位及斜冠状位扫描,扫描范围从骨盆上缘至髋臼,扫描序列包括常规横轴位T1WI、T2WI以及斜冠状位PDWI-fs,并加扫斜冠状位T1-mapping扫描,TR 11 ms,TE 1.57 ms,flip angle 5°、27°,FOV 240 mm×240 mm,矩阵256×256,层厚3.0 mm,层数22 (3D SCAN),间隔0.6 mm,iPAT因子2,扫描时间 2 min 7 s。

1.3 弛豫时间值的测量

       扫描完成后自动生成T1-mapping伪彩图。由两名高年资从事磁共振诊断10年的主治医师分别在Siemens syngo MRD 13图像后处理工作站上,进行相应的伪彩图与斜冠状位PDWI-fs图像融合处理。手动将感兴趣区ROI放置在骶髂关节的相应区域,ROI尽量靠近关节软骨,但不包括关节软骨,且应该远离血管、骨皮质等区域。以常规MRI序列为参照,骶髂关节分为四个软骨下部分(左髂骨、左骶骨、右髂骨和右骶骨),每个软骨下部分放置3个感兴趣区。为了指导ROI的放置,读者评估了骶髂关节是否存在骨髓水肿(bone marrow edema,BME)作为活动性炎症改变的标志。如果读者在PDWI-fs上发现高信号区,则认为存在BME。如果在软骨下骨检出BME,则在PDWI-fs上信号强度最高的T1-mapping伪彩图上放置3个互不重叠的感兴趣区(25~30 mm2)。如果未检测到BME,则将3个感兴趣区放置在上、中、下软骨下骨髓上。通过这个过程,从每个患者两侧骶髂关节的T1-mapping伪彩图中获得6个感兴趣区域,取骶侧和髂侧6个区域的平均值作为最终值。测量数据差异较大时,经协商后测量同一层面同一位置分别进行测量,形成最后一致结果。

1.4 统计学分析

       利用SPSS 25.0进行数据分析,对计量资料进行正态性检验:服从正态分布,采用(x¯±s)表示;不服从正态分布,采用Median (Q1,Q3)表示。运用秩和检验对对照组和病例组以及各亚组骶髂关节软骨下骨髓的T1-mapping值进行比较,并进行受试者工作特征(receiver operating characteristic,ROC)曲线分析诊断效能;采用Kruskal-Wallis H检验对活动组3个亚组的变量进行统计学差异性分析;采用配对t检验对治疗组中各组 T1-mapping值下降率进行比较。检验水平α=0.05,P<0.05为差异有显著统计学意义。

2 结果

2.1 ASDAS评分及常规MRI表现

       由两名高年资风湿免疫科的主治医师对对照组、病例组及其亚组、治疗组进行ASDAS评分,评分结果差异较大时,经协商后重新进行评分,形成最后一致结果(表1)。

       axSpA患者骶髂关节MRI表现主要包括不同程度的关节软骨下骨髓水肿及脂肪沉积、骨质的侵蚀与破坏,随着患者骶髂关节炎症水肿程度加重,ASDAS评分增加,压脂PDWI序列表现为骶髂关节软骨下骨髓的信号不同程度增高,随着治疗周期增加,患者的ASDAS评分减低,压脂PDWI序列表现为骶髂关节软骨下骨髓的信号不同程度减低(图1A1B1C1D)。

图1  男,27岁,骶髂关节炎,HLA-B27:+,首诊CRP:31.5 mg/L,ESR:25 mm/h,ASDAS:4.6,属于活动度非常高组。1A~1D:PDWI 冠状位图;1E~1H:T1-mapping冠状位伪彩图。1A:治疗前PDWI冠状位提示双侧骶髂关节关节面下骨质见边界模糊的斑片状高信号,以右侧中下部为著,相应关节面欠光整;1E:病灶感兴趣区平均T1-mapping值为1075.37 ms;1B和1F (治疗三周)、1C和1G (治疗六周)、1D和1H (治疗十二周):提示患者双侧骶髂关节关节面下高信号较前逐步降低,T1-mapping值分别为480.03 ms、410.67 ms、311.63 ms。
Fig. 1  Male, 27, axSpA, HLA-B27: +, CRP: 31.5 mg/L,ESR: 25 mm/h,ASDAS: 4.6, belongs to the very high activity group. Fig. 1A-1D: the coronal plane of PDWI, Fig. 1E-1H: T1-mapping coronary pseudo color map. Fig. 1A (the coronal plane of PDWI): the bone under bilateral sacroiliac joint subchondral showed patchy high signal with fuzzy boundary, especially in the middle and lower part of the right side, and the corresponding joint surface was not smooth, the average T1-mapping value of the focus interest area in Fig. 1E was 1075.37 ms. Fig. 1B, 1F (three weeks of treatment), Fig. 1C, 1G (six weeks of treatment), Fig. 1D, 1H (12 weeks of treatment) suggested that the signal of the patients' bilateral sacroiliac joint was lower than that before, and T1-mapping value of the region of interest decreased (480.03 ms, 410.67 ms, 311.63 ms). The value of T1-mapping decreased synchronously with the value of ASDAS-CRP.
表1  患者临床资料及病情活动度评分(ASDAS)
Tab. 1  ASDAS-CRP score in each group

2.2 骶髂关节骶侧、髂侧关节软骨下骨髓区T1-mapping值组内对比

       经检验对照组以及病例组中非活动组、活动组骶髂关节骶侧、髂侧T1-mapping值不符合正态分布,各组间骶侧、髂侧T1-mapping值差异无统计学意义,见表2

表2  各组骶髂关节骶侧、髂侧T1-mapping值及差异性对比
Tab. 2  Comparison of sacroiliac joint T1-mapping value and difference

2.3 骶髂关节骶侧、髂侧关节软骨下骨髓含水量T1-mapping值组间对比

       病例组T1-mapping值高于对照组,病例组中活动组T1-mapping值高于非活动组(表2)。不论选择骶侧还是髂侧为分析对象,T1-mapping值在对照组vs.病例组、对照组vs.非活动组、对照组vs.活动组、非活动组vs.活动组间差异均有统计学意义(表3)。

       T1-mapping值在对照组和病例组、对照组和非活动组间、对照组和活动组间、非活动组和活动组均具有最好的诊断效能(表4)。

表3  骶髂关节骶侧、髂侧T1-mapping值在各组间差异性比较
Tab. 3  Comparison of T1-mapping value of sacral and iliac of sacroiliac joint among different groups
表4  骶髂关节骶侧、髂侧T1-mapping值诊断效能比较
Tab. 4  Comparison of diagnostic efficacy of sacroiliac joint sacral and iliac T1-mapping values

2.4 活动组三个亚组间骶髂关节软骨下骨髓含水量T1-mapping值对比

       比较活动组三个亚组间的分布差异,三个亚组中T1-mapping值(中位数)见表5。采用Kruskal-Wallis H检验,各组T1-mapping值差异具有统计学意义(髂侧H=11.496、P=0.003;骶侧H=11.954、P=0.003)。采用Bonferroni法校正显著性水平的事后两两比较发现,T1-mapping值在中度活动组和活动度非常高组间(调整后骶侧P=0.004、髂侧P=0.002)、活动度提高组和活动度非常高组间(调整后骶侧P=0.018、骶侧P=0.029)差异具有统计学意义,而中度活动组和活动度提高组间(调整后骶侧P=0.878、髂侧P=0.494)差异不具有统计学意义。

表5  活动组亚组间骶髂关节骶侧、髂侧T1-mapping值比较
Tab. 5  Comparison of T1-mapping value of sacroiliac joint between subgroups of the activity group

2.5 治疗组骶髂关节软骨下骨髓区T1-mapping值下降率的比较

       与治疗前对比,治疗3周组、治疗6周组及治疗12周组骨髓T1-mapping值均下降(图1E1F1G1H),T1-mapping值下降率平均值分别为(0.360±0.203、0.551±0.129、0.658±0.098),经检验T1-mapping值下降率符合正态分布,运用配对t检验分别比较治疗3周组和治疗6周组、治疗6周组和治疗12周组骨髓T1-mapping值下降率,t分别为(-5.978、-6.778),P均<0.001,故三组间差异具有显著统计学意义。

3 讨论

       axSpA临床发病率较高且致残率高,极大影响患者的生活质量和劳动能力,是较严重的公共卫生问题,控制并降低疾病活动状态从而改善患者的生活质量是目前临床治疗的主要目标。TNF-α在axSpA的发病机制中起到重要作用,尤其是在促进炎症反应过程中,TNF-α拮抗剂(TNFi)能有效降低血中TNF-α水平,从而控制炎症、降低axSpA疾病活动状态、延缓axSpA进展、改善预后。目前临床上TNFi治疗axSpA的疗效已获充分证据,成为活动期强直性脊柱炎患者的一线用药[4, 5, 6],2016年由ASAS/EULAR联合制定的SpA指南中推荐对于炎症持续缓解的患者可考虑TNFi减量[10],因此如何实时有效评估axSpA患者治疗后疾病活动状态,对及时调整临床治疗方案及减轻患者经济负担都有着积极意义。随着软硬件技术的发展,越来越多功能磁共振检查技术应用于骶髂关节研究[11, 12]。MRI T1-mapping技术可反映组织中水和细胞外基质分子间慢频率的相互作用,并将细微的水分子改变以T1-mapping值的形式定量体现[7, 8]。本研究运用T1-mapping技术定量评估axSpA骶髂关节软骨下骨髓水肿程度,并运用治疗组不同治疗周期T1-mapping值下降率对疗效进行监测,有望对axSpA炎症活动性和疗效监测提供有效的定量指标。

3.1 axSpA活动性骶髂关节炎常见评价方法及局限性

       目前临床上对axSpA活动性评价常用ASDAS评分,是2009年推出新的强直性脊柱炎疾病活动度评分,是第一个综合了患者主观评价及实验室的客观指标的疾病活动性评分系统,对疾病的鉴别能力和敏感度均优于单一参数,是目前最精准的与axSpA脊柱影像学进展相关的疾病活动性指标[13, 14],但其计算依然需要依靠患者主观评价而影响准确性。

       常用的影像学检查方法包括X线平片、CT检查[15]、放射性核素显像[16]、多普勒超声[17, 18]等,这些检查多为结构成像,虽有助于axSpA定性诊断,但对于axSpA早期常表现为假阴性,而且对其axSpA炎症活动性的评估存在较大局限。MRI STIR序列作为常规诊断骶髂关节炎的检查手段,具有较高的敏感度和特异度,能直接显示其他影像技术无法显示的关节软骨异常、关节软骨下骨髓水肿、脂肪沉积,有利于早期发现和诊断骶髂关节炎,并用于监测病情发展[19, 20]。目前常规STIR序列基本能满足axSpA活动性骶髂关节炎的诊断,但STIR序列图像仍然仅为一种形态学成像,对于疾病状况的反映仍较病理改变滞后,且不能对炎症程度准确量化。

3.2 T1-mapping量化成像技术及临床运用

       早期骶髂关节改变主要表现为滑膜炎和关节软骨下骨髓炎症,血管扩张,引起骨髓血管翳,炎性细胞浸润,炎性因子激活,进一步加剧炎症反应链,这也是影像学提示骨髓水肿与疾病活动状态相关性的病理学基础。

       T1-mapping成像技术反映组织中水和细胞外基质分子间慢频率的相互作用,对组织内蛋白多糖含量变化敏感,不依赖于参考组织的信号强度,既往用于对心肌组织水肿和纤维化程度进行定量[21],因组织的T1值较为独立,不受胶原排列方向的影响,也用于关节软骨生化成像[7, 8]。通过T1-mapping值对骶髂关节软骨下骨髓水肿程度进行定量,可以反映骨髓内在的特性和水含量的变化。

       目前国内外对此的探讨较少,T1-mapping技术可以检测组织中水分子的微小变化,定量评估axSpA骶髂关节软骨下骨髓水肿程度,在骨髓水肿的诊断效能中具有很好的敏感度,诊断的准确度和特异度较高。本研究显示,病例组中非活动组和活动组T1-mapping值均高于对照组,提示临床上所定义的非活动期仍可能出现骶髂关节软骨下骨髓水肿;有研究[22, 23]表明MRI观察到骶髂关节软骨下骨髓水肿是证明axSpA活动性的关键,随着病情加重,患者ASDAS评分增加,相应的骶髂关节骨髓水肿程度增加,STIR序列表现为骶髂关节面下骨髓的信号不同程度增高,T1-mapping值也相应升高;在本研究中活动组T1-mapping值高于对照组,并且在活动组中随着疾病活动度的提高,相应的弛豫时间值也升高。

       TNFi通过结合血清中TNF-α,阻断TNF-α与细胞表面TNF-α受体的结合,抑制由TNF-α受体介导的异常免疫反应及炎症过程,能有效地控制炎症和降低axSpA疾病活动状态。本研究显示,随着治疗周期增加,患者ASDAS评分减低,压脂PDWI序列表现为骶髂关节面下骨髓的信号不同程度减低,患者骶髂关节骨髓T1-mapping值下降,治疗组中不同治疗周期的骶髂关节软骨下骨髓T1-mapping值的下降率随着治疗周期的延长而进一步增加,且组间差异具有显著统计学意义,说明T1-mapping值的下降率在监测患者TNFi疗效中具有一定指导意义。笔者认为T1-mapping定量技术对于水含量的精确测量或可帮助临床准确评估早期骶髂关节炎水肿,并在患者治疗过程中能实时检测患者骨髓水肿变化的情况。

4 研究的局限性

       (1) axSpA骶髂关节炎是由多种因素造成的,所引起的骶髂关节病理改变过程复杂,包括骨髓水肿和脂肪沉积等,本研究采用T1-mapping技术分析骶髂关节软骨下骨髓水肿的改变,未进行其他因素影响的综合分析。(2)本研究以临床上ASDAS评分作为AS治疗后活动状态评估的标准,缺乏病理金标准的指导。(3)针对治疗患者初始axSpA活动状态有一定程度的差异,未进行精确的分组,不同活动状态的患者治疗效果可能有所差异。(4)未对临床症状缓解后复发患者进一步分析,需要长期随访患者进一步证实。

5 结论

       T1-mapping技术可用于骶髂关节检查,为中轴型脊柱关节炎骶髂关节活动性病变临床诊断及疗效评估提供有效定量指标,有益于临床个体化治疗、及时调整治疗方案。

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