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• 临床研究 •
扩散张量成像对新生儿急性胆红素脑病神经核团及脑白质纤维的分析研究
牛劲 闫瑞芳 殷慧佳 任继鹏 岳征 谢北辰 韩东明

Cite this article as: NIU J, YAN R F, YIN H J, et al. Study of cerebral nuclei and white matter fibers in neonatal acute bilirubin encephalopathy based on diffusion tensor imaging[J]. Chin J Magn Reson Imaging, 2023, 14(1): 67-71.本文引用格式：牛劲, 闫瑞芳, 殷慧佳, 等. 扩散张量成像对新生儿急性胆红素脑病神经核团及脑白质纤维的分析研究[J]. 磁共振成像, 2023, 14(1): 67-71. DOI:10.12015/issn.1674-8034.2023.01.012.


[摘要] 目的 探讨扩散张量成像（diffusion tensor imaging, DTI）对急性胆红素脑病（acute bilirubin encephalopathy, ABE）神经核团及脑白质纤维束的研究价值。材料与方法 选取30例ABE足月新生儿作为病变组，对照组选取30例正常足月新生儿，行常规MRI和DTI检查。测量双侧额叶运动皮层、额叶深部白质、侧脑室体上方白质、丘脑腹侧核、苍白球、内囊后肢、胼胝体压部、丘脑底核、红核/黑质、脑桥核、海马、延髓核及小脑齿状核DTI参数，包括平均扩散系数（average diffusion coefficient, ADC）、各向异性分数（fractional anisotropy, FA）及各向同性（isotropy, Iso）值，分别进行统计学分析。结果 与对照组相比，病变组双侧额叶运动皮层、内囊后肢、齿状核ADC、Iso值下降，FA值升高（P＜0.05）；病变组双侧脑室体上方白质、苍白球、胼胝体压部、红核/黑质、脑桥核、海马Iso值下降（P＜0.05）。两组相比双侧额叶深部白质、丘脑腹侧核、丘脑底核延髓核ADC、FA和Iso值差异均无统计学意义（P＞0.05）。结论 DTI提示了ABE可能同时存在神经核团及脑白质纤维损伤。
[Abstract] Objective To investigate the value of diffusion tensor imaging (DTI) in the study of cerebral nuclei and white matter fibers in acute bilirubin encephalopathy (ABE).Materials and Methods Thirty full-term neonates with ABE were selected as the lesion group, and 30 normal full-term neonates were selected as the control group. All of them were examined by conventional MRI and DTI. The average diffusion coefficient (ADC), fractional anisotropy (FA) and isotropy (Iso) values of bilateral frontal lobe motor cortex, deep frontal lobe white matter, white matter above lateral ventricle, ventral thalamic nucleus, globus pallidus, posterior limb of internal capsule, splenium corporis callosi, subthalamic nucleus, red nucleus/substantia nigra, pontine nucleus, hippocampus, medulla oblongata and cerebellar dentate nucleus were measured and statistically analyzed respectively.Results Compared with the control group, ADC and Iso values were lower and FA values were higher in the bilateral frontal lobe motor cortex, posterior limb of internal capsule and dentate nucleus of the lesion group (P＜0.05). And Iso values were lower in the bilateral white matter above bilateral lateral ventricle,globus pallidus, splenium corporis callosi, red nucleus/substantia nigra, pontine nucleus and hippocampus of the lesion group (P＜0.05). There were no significant statistical difference in ADC, FA and Iso values in the bilateral frontal lobes deep white matter, ventral thalamic nucleus,subthalamic nucleus and medulla oblongata (P＞0.05).Conclusions DTI suggests that the injury of cerebral nuclei and white matter fibers in ABE.
[关键词] 胆红素脑病；新生儿；神经通路；扩散张量成像；磁共振成像
[Keywords] bilirubin encephalopathy；neonate；neural pathway；diffusion tensor imaging；magnetic resonance imaging

牛劲    闫瑞芳 *   殷慧佳    任继鹏    岳征    谢北辰    韩东明   

新乡医学院第一附属医院磁共振科，新乡　453100

通信作者：闫瑞芳，E-mail：yrf718@163.com

作者贡献声明：闫瑞芳设计本研究的方案，获取、分析或解释本研究的数据，对稿件重要的智力内容进行了修改；牛劲起草和撰写稿件，获取、分析或解释本研究的数据；殷慧佳、任继鹏、岳征、谢北辰、韩东明获取、分析或解释本研究的数据，对稿件重要的智力内容进行了修改；全体作者都同意发表最后的修改稿，同意对本研究的所有方面负责，确保本研究的准确性和诚信。


基金项目： 河南省医学科技攻关计划项目 LHGJ20200519
收稿日期：2022-09-12
接受日期：2022-11-29
中图分类号：R445.2  R722.17 
文献标识码：A
DOI: 10.12015/issn.1674-8034.2023.01.012
本文引用格式：牛劲, 闫瑞芳, 殷慧佳, 等. 扩散张量成像对新生儿急性胆红素脑病神经核团及脑白质纤维的分析研究[J]. 磁共振成像, 2023, 14(1): 67-71. DOI:10.12015/issn.1674-8034.2023.01.012.

0 前言

       胆红素脑病（bilirubin encephalopathy, BE）可造成新生儿严重神经系统后遗症，对BE的早期诊断及治疗是改善预后的关键[1]。急性胆红素脑病（acute bilirubin encephalopathy, ABE）常规MRI表现为双侧苍白球和丘脑底核对称性T1WI信号增高[2, 3]。扩散张量成像（diffusion tensor imaging, DTI）对于脑白质的结构变化非常敏感，能够观察到早期的脑白质细微病变[4]。近年来DTI广泛应用于孤独症谱系障碍、多动症及抑郁症等疾病的研究[5, 6]。对于ABE新生儿在DTI的研究报道较少，有研究表明高胆红素血症患儿苍白球、内囊后肢FA值明显下降[7]。在BE时，易受到胆红素毒性影响的区域包括苍白球、黑质、海马、丘脑及小脑齿状核[8, 9]，这些皮层下区域通过众多的白质连接，彼此相互联系。但现有ABE新生儿DTI研究使用的DTI参数单一，且胆红素毒性易损区域尚未得到充分研究，这些神经核团及脑白质纤维束在BE中的变化仍不清楚[7,10]。本研究旨在通过常规MRI及DTI，分析ABE新生儿胆红素毒性对神经核团及脑白质纤维的影响。

1 材料与方法

1.1 一般资料

       本研究符合2013年版《赫尔辛基宣言》，通过新乡医学院第一附属医院伦理委员会批准（批准文号：2020040），所有新生儿监护人均知情同意本研究内容。病变组：2014年7月至2021年12月间在我院住院的高胆红素血症足月新生儿30例，其中男16例（53.33%），接受MRI检查的日龄为3～13（7.61±4.08）d。排除合并先天性颅脑发育不良、新生儿窒息、病毒性脑炎等疾病，所有患儿血清总胆红素峰值超过342 μmol/L（20 mg/dL），常规MRI双侧苍白球T1WI信号对称性增高，且符合临床诊断ABE标准[11]。对照组：正常足月新生儿30例，其中男15例（50.00%），接受MRI检查的日龄为3～12（7.15±4.51）d，所有新生儿血清总胆红素均小于205 μmol/L，排除脑部疾病、先天畸形等患儿。

1.2 检查方法

       扫描前均采用水合氯醛进行灌肠处理，镇静成功30 min内完成检查。MRI检查选用GE 3.0 T（Signa Excite）超导MR及8通道头颈联合线圈，行头颅常规MRI及DTI检查。常规MRI包括轴位及矢状位T1WI、轴位T2WI、轴位T2 FLAIR、轴位DWI。DTI检查采用单次激发自旋回波-回波平面成像（spin-echo echo planar imaging, SE-EPI）序列，扫描参数如下：TR 9000 ms，TE 107 ms，层厚3 mm，层间距0，FOV 20 cm×20 cm，NEX 2，矩阵128×128，b＝0、1000 s/mm2，扩散敏感梯度场施加方向15个。

1.3 图像分析

       图像后处理在ADW 4.6工作站进行，应用Functool后处理软件，结合平均扩散系数（average diffusion coefficient, ADC）图和各向同性（isotropy, Iso）图，在各向异性分数（fractional anisotropy, FA）图上勾画椭圆形感兴趣区，感兴趣区的设置要求放在目标测定解剖结构的中心，大小范围在20～30 mm2，感兴趣区包括：双侧额叶运动皮层（中央前回）、额叶深部白质、侧脑室体上方白质、丘脑腹侧核、苍白球、内囊后肢、胼胝体压部、丘脑底核、红核/黑质、脑桥前中部两侧核团区、海马、延髓前部两侧核团区、小脑齿状核，分别测量各感兴趣区的ADC、FA及Iso值（图1）。胼胝体膝部分别在左右侧各选一个感兴趣区。由于红核/黑质体积较小，感兴趣区无法细分，因此在一个感兴趣区内进行测量。感兴趣区的测量方法见图1。各感兴趣区的ADC值、FA值和Iso值重复测量3次，取平均值作为相应区域的ADC值、FA值和Iso值，以减少测量误差。

图1  男，13 d，血清总胆红素370.5 μmol/L。1A～1H为感兴趣区对应的各向异性分数（FA）图。1A：双侧额叶运动皮层及深部白质；1B：双侧额叶侧脑室体部上方白质；1C：双侧丘脑腹侧核；1D：双侧额叶白质、苍白球、内囊后肢、胼胝体压部；1E：双侧丘脑底核；1F：双侧红核/黑质；1G：脑桥核及双侧海马；1H：延髓核及小脑齿状核。1I：T1WI双侧苍白球、丘脑底核信号增高。1J：扩散加权成像（DWI）图未见异常。
Fig. 1  Male, 13 days old, full-term newborn with serum total bilirubin 370.5 μmol/L. The pictures of 1A-1H are fractional anisotropy (FA) map corresponding to the ROIs. 1A: Motor cortex and deep white matter of bilateral frontal lobes; 1B: Bilateral frontal lobe white matter above bilateral lateral ventricle; 1C: Bilateral ventral thalamic nucleus; 1D: Bilateral frontal lobes white matter, bilateral globus pallidus, bilateral posterior limb of internal capsule, splenium corporis callosi; 1E: Bilateral subthalamic nucleus; 1F: Bilateral red nucleus/substantia nigra; 1G: Pontine nucleus, bilateral hippocampus; 1H: Medulla oblongata, cerebellar dentate nucleus. 1I: The increased T1WI signal of bilateral globus pallidus and subthalamic nucleus. 1J: There is no abnormality in diffusion-weighted imaging (DWI).

1.4 统计学方法

       应用SPSS 25.0统计软件进行数据分析，计量资料采用方差分析，计量资料以均数±标准差的形式来表示；两组间比较采用t检验，P＜0.05表示差异有统计学意义。

2 结果

2.1 病变组与对照组头颅常规MRI比较

       病变组的30例ABE新生儿，T1WI均表现双侧苍白球信号对称性增高，T2WI及DWI均未见异常信号（图1）。对照组30例，头颅MRI全部未见异常。

2.2 病变组与对照组各感兴趣区的DTI参数比较

       与对照组相比，病变组双侧额叶运动皮层、内囊后肢、齿状核ADC、Iso值下降，FA值升高（P＜0.05）（表1～3）；病变组双侧侧脑室体上方白质、苍白球、胼胝体压部、红核/黑质、脑桥核、海马Iso值下降（P＜0.05），ADC、FA值差异无统计学意义（P＞0.05）（表4～6）。两组相比双侧额叶深部白质、丘脑腹侧核、丘脑底核、延髓核ADC、FA、Iso值差异均无统计学意义（P＞0.05）（表7～9）。

表1  双侧额叶运动皮层、内囊后肢、齿状核ADC值
Tab. 1  The statistical results of ADC value in the bilateral frontal lobe motor cortex, posterior limb of internal capsule and dentate nucleus
表2  双侧额叶运动皮层、内囊后肢、齿状核FA值
Tab. 2  The statistical results of FA value in the bilateral frontal lobe motor cortex, posterior limb of internal capsule and dentate nucleus
表3  双侧额叶运动皮层、内囊后肢、齿状核Iso值
Tab. 3  The statistical results of Iso value in the bilateral frontal lobe motor cortex, posterior limb of internal capsule and dentate nucleus
表4  双侧侧脑室体上方白质、胼胝体压部、苍白球、红核/黑质、海马、脑桥核ADC值
Tab. 4  The statistical results of ADC value in the bilateral white matter above bilateral lateral ventricle, splenium corporis callosi, globus pallidus, red nucleus/substantia nigra, hippocampus and pontine nucleus
表5  双侧侧脑室体上方白质、胼胝体压部、苍白球、红核/黑质、海马、脑桥核FA值
Tab. 5  The statistical results of FA value in the bilateral white matter above bilateral lateral ventricle, splenium corporis callosi, globus pallidus, red nucleus/substantia nigra, hippocampus and pontine nucleus
表6  双侧侧脑室体上方白质、胼胝体压部、苍白球、红核/黑质、海马、脑桥核Iso值
Tab. 6  The statistical results of Iso value in the bilateral white matter above bilateral lateral ventricle, splenium corporis callosi,globus pallidus, red nucleus/substantia nigra, hippocampus and pontine nucleus
表7  双侧额叶深部白质、丘脑腹侧核、丘脑底核、延髓核ADC值
Tab. 7  The statistical results of ADC value in the bilateral frontal lobes deep white matter, ventral thalamic nucleus, subthalamic nucleus and medulla oblongata
表8  双侧额叶深部白质、丘脑腹侧核、丘脑底核、延髓核FA值
Tab. 8  The statistical results of FA value in the bilateral frontal lobes deep white matter, ventral thalamic nucleus, subthalamic nucleus and medulla oblongata
表9  双侧额叶深部白质、丘脑腹侧核、丘脑底核、延髓核Iso值
Tab. 9  The statistical results of Iso value in the bilateral frontal lobes deep white matter, ventral thalamic nucleus, subthalamic nucleus and medulla oblongata

3 讨论

       胆红素对神经系统的损伤机制目前尚不明确，有研究显示胆红素的神经毒性可能与Ca2+依赖的电压门控钠通道有关[12]。胆红素引起神经元和神经胶质细胞受损时，神经纤维可出现一定程度的髓鞘化不良[13]。DTI可通过评估白质束中水扩散的动力学来检查脑白质微观结构[4]。本研究通过不同DTI参数分析组织内部水分子扩散运动的速度及方向，提示了ABE患儿的胆红素神经毒性可能引起神经核团及脑白质纤维损伤。

       胆红素主要选择性沉积在苍白球、基底节、黑质、海马、丘脑、齿状核和小脑[14, 15]。DTI技术利用水分子的不规则自由运动来激发EPI序列，反映神经纤维的微观结构，检测脑白质纤维束的完整性[6,16]。本研究中与对照组相比，病变组双侧额叶运动皮层、内囊后肢、齿状核ADC值下降，FA值升高，提示水分子扩散运动受限[17, 18]，可能表明水从细胞外进入细胞内，或降低了细胞膜的通透性，限制细胞内水分扩散，从而引起细胞肿胀[19, 20]；导致上述脑区中有髓神经纤维之间的间隙变窄，限制了水分子在纤维束上的运动[21]。同时SHAPIRO等[22]认为ADC的减少可能也反映了细胞内稳态的破坏，说明这些区域细胞稳态发生了变化，这可能会引起细胞毒性水肿。病变组双侧额叶运动皮层、侧脑室体部上方白质、苍白球、内囊后肢、胼胝体压部、红核/黑质、脑桥核、海马、齿状核Iso值下降，提示这些脑区组织内各向同性下降，局部脑组织的自由水减少[23]，这可能反映了胆红素毒性影响这些脑区的髓鞘再生过程，提示轴突间室内改变和组织内自由水减少[24, 25]。此外，病变组苍白球的T1WI信号强度普遍增加，但ADC、FA值差异无统计学意义，说明细胞稳态不受影响，胆红素沉积不会导致苍白球细胞毒性水肿的发生。

       两组相比，双侧额叶深部白质、丘脑腹侧核、丘脑底核、延髓核ADC、FA、ISO值差异均无统计学意义。说明胆红素可能对上述区域水分子扩散影响不大，不易造成持久的脑损伤。慢性BE的婴儿常显示双侧苍白球对称性的T2WI异常高信号，而丘脑底核很少有异常信号持续存在[26, 27, 28]，或许可以通过本研究来解释。WISNOWSKI等[29]研究表明ABE患儿丘脑水分子扩散受限，但本研究中病变组与对照组丘脑腹侧核、丘脑底核ADC、FA、Iso值差异均无统计学意义，原因可能是本研究中的病变组血清总胆红素水平相对较低[30]，胆红素毒性对丘脑的影响较小。

       本研究还存在一些不足之处：首先样本量相对较小，待日后继续收集整理；其次手动绘制感兴趣区，测量误差难以避免。

4 结论

       综上所述，ABE患儿和对照组的脑内额叶运动皮层、内囊后肢、齿状核等部位DTI参数存在差异，DTI对 ABE有很高的研究价值，能够为ABE胆红素毒性对神经核团及脑白质纤维损伤的研究提供可靠的客观依据。

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