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临床研究
孕中晚期胎儿海马折叠角变化的产前MRI研究
孙悦 曹一民 伊泽茜 孟卫新 周立霞

Cite this article as SUN Y, CAO Y M, YI Z X, et al. Prenatal MRI of fetal hippocampal infolding angle change in middle and third trimester[J]. Chin J Magn Reson Imaging, 2024, 15(5): 24-27, 101.本文引用格式孙悦, 曹一民, 伊泽茜, 等. 孕中晚期胎儿海马折叠角变化的产前MRI研究[J]. 磁共振成像, 2024, 15(5): 24-27, 101. DOI:10.12015/issn.1674-8034.2024.05.005.


[摘要] 目的 应用产前MRI研究孕中晚期胎儿海马折叠角(hippocampal infolding angle, HIA)的变化规律。材料与方法 回顾性分析在河北医科大学第二医院2018年1月至2021年12月行产前MRI检查的孕中晚期正常胎儿影像学资料。于胎儿颅脑MRI的稳态采集快速成像(fast imaging employing steady state acquisition, FIESTA)序列冠状切面测量HIA,统计分析中晚孕期胎儿HIA的正常值范围,探讨其与孕龄变化的相关性以及临床应用价值。结果 共有139例孕中晚期胎儿纳入研究,孕周20~38(29.17±3.90)周,男胎∶女胎=105∶34。按孕龄分为6组,分析得到胎儿海马折叠角的置信区间。随着孕龄增加,左右两侧HIA均呈线性增大(R2=0.803、0.836,P均<0.001),且右侧HIA大于左侧,但未发现左右两侧存在性别间差异(P=0.898)。结论 产前MRI发现孕中晚期胎儿HIA的变化具有一定的规律,可为宫内或生后与海马结构异常相关的疾病提供影像学诊断依据。
[Abstract] Objective Prenatal MRI was used to study the changes of the hippocampal infolding angle (HIA) of fetuses in the second and third trimester of pregnancy.Materials and Methods The imaging data of normal fetuses in the second and third trimester of pregnancy undergoing prenatal MRI in the Second Hospital of Hebei Medical University from January 2018 to December 2021 were collected and were retrospectively analyzed. HIA in the coronal section of fetal brain MRI using the fast imaging employing steady state acquisition (FIESTA) sequence was measured, the normal range of HIA in fetuses in the second and third trimester of pregnancy was analyzed, to explore its correlation with gestational age changes and clinical application value.Results A total of 139 cases of fetuses in the second and third trimester of pregnancy were included in the study, with a gestational age ranging from 20 to 38 weeks (mean 29.17±3.90 weeks), and a male-to-female ratio of 105∶34. The data was divided into 6 groups based on gestational age, and the confidence interval of fetal HIA was analyzed. With increasing gestational age, the HIA on both sides increased linearly (R2=0.803, 0.836, both P<0.001), and the HIA on the right side was greater than that on the left side. However, no gender differences were found in the left and right sides (P=0.898).Conclusions Prenatal MRI revealed that the changes of the HIA in fetuses in the second and third trimester of pregnancy follows a certain pattern, which can provide imaging diagnostic evidence for diseases related to hippocampal structural abnormalities either in utero or after birth.
[关键词] 胎儿;海马折叠角;磁共振成像;发育;海马结构
[Keywords] fetus;hippocampal infolding angle;magnetic resonance imaging;development;hippocampal structure

孙悦    曹一民    伊泽茜    孟卫新    周立霞 *  

河北医科大学第二医院影像科,石家庄 050051

通信作者:周立霞,E-mail:doctorzhou@126.com

作者贡献声明::周立霞设计本研究的方案,对稿件重要的内容进行了修改;孙悦起草和撰写稿件,获取、分析和解释本研究的数据;曹一民、伊泽茜、孟卫新获取、分析和解释本研究的数据,对稿件重要的内容进行了修改;周立霞获得了北京康盟慈善基金会医学科研发展基金项目伦琴影像科研专项的资助;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: 北京康盟慈善基金会医学科研发展基金伦琴影像科研专项 HB-201906-003
收稿日期:2024-01-14
接受日期:2024-04-17
中图分类号:R445.2  R714.5 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2024.05.005
本文引用格式孙悦, 曹一民, 伊泽茜, 等. 孕中晚期胎儿海马折叠角变化的产前MRI研究[J]. 磁共振成像, 2024, 15(5): 24-27, 101. DOI:10.12015/issn.1674-8034.2024.05.005.

0 引言

       人脑海马的主要功能与记忆、学习、情感以及方向定位等有关,是近年来神经疾病学科研究的热点。海马是人脑边缘系统的重要组成部分,在情绪、记忆和内脏活动中发挥重要功能。胎儿期海马的发育较为复杂,一些出生后的疾病如儿童癫痫与胎儿期海马旋转异常和宫内海马损伤有关[1, 2]。超声是产前影像学检查的首选方法,且有产前超声研究发现胎儿海马的二维径线及体积随着孕龄的增长而增加[3],但超声图像易受到孕妇过于肥胖、合并子宫肌瘤、羊水过少、子宫畸形、双胎、多胎、孕周过大、胎儿体位及胎儿骨骼骨化等因素的影响,而胎儿MRI不受以上因素的影响,组织分辨率高,可进行大范围、多参数成像,对胎儿脑实质细小结构的观察更具优势,现已逐渐胎儿疾病的诊断,可用于评估胎儿的脑发育[4]

       海马结构主要由齿状回、海马角、下托以及相关的白质结构如海马伞、海马神经纤维等构成[5, 6]。在胎儿的大脑发育过程中,海马的齿状回及海马角体积逐渐增大,进而旋转折叠进入颞叶,海马形态发生变化。HIA是连接海马下托内侧面上缘与海马角的外侧缘连线和大脑半球垂直中线之间的角度,随着海马的发育,HIA会发生变化,其在一定程度上可以作为海马发育的参考值之一[7]

       目前关于胎儿期正常海马发育相关的MRI研究较少。部分学者对欧美国家宫内孕中晚期胎儿海马发育进行过MRI形态研究[8, 9],国内与胎儿期海马发育相关的MRI研究仅限于中孕期的引产后胎儿。考虑到胎儿标本制作过程中的脱水固定等流程的影响及样本量较少等因素可能对HIA的测量结果造成误差[10]。在体测量可能更准确,但是目前国内尚无孕中晚期正常在体胎儿海马发育的MRI影像数据。本文以回顾性分析的研究方式,通过对孕中晚期正常在体胎儿HIA的测量,分析其与孕龄变化的关系,旨在探究孕期胎儿HIA值的变化规律,间接反映海马的发育特征,为临床产前和围产期相关疾病的筛查和诊断提供一定依据。

1 材料与方法

1.1 研究对象

       本研究遵守《赫尔辛基宣言》,并经河北医科大学第二医院伦理委员会批准,免除受试者知情同意,科研伦理审批号:2016164。回顾性分析河北医科大学第二医院2018年1月至2021年12月因产前超声怀疑胎儿有轻微非中枢神经系统异常而接受MRI检查的孕妇资料。纳入标准:(1)孕20~38周;(2)单胎妊娠;(3)胎儿MRI检查未见异常;(4)出生后1年内MRI或临床Gesell评分证实中枢神经系统无异常。排除标准:(1)孕妇年龄<18岁;(2)孕妇合并妊娠期并发症(如妊娠期高血压、糖尿病等);(3)MRI图像质量未满足研究要求;(4)胎儿脑或其他器官发育异常者。

1.2 扫描设备与参数

       检查仪器为GE Signa 1.5 T MR扫描仪。检查前告知孕妇扫描的整个过程中及注意事项。孕妇体位采取仰卧或侧卧,足先进,8通道体部相控阵线圈进行检查,线圈下垫薄垫,防止直接接触孕妇体表。常规采集胎儿脑横断面、冠状面及矢状面。扫描序列均为快速序列:单次激发快速自旋回波序列,TE 140 ms,TR 2000 ms;FIESTA序列,TE 2.3 ms,TR 5.3 ms;弥散加权成像序列,b值为700 s/mm2。以上三个序列层厚均5 mm,负间隔扫描均为-3 mm,FOV均为380 mm×380 mm。

1.3 图像分析

       将每例胎儿的MRI图像进行分析,根据图像清晰度,选择对于海马结构显像较好的FIESTA序列冠状面测量HIA。在二维图像上利用Syngo Plaza软件观察对海马结构的形态进行精准识别,参考RIGHINI等[7]的文献,在经过脑桥的冠状面上测量HIA[11]图1),以手动画出海马的折叠角的两条边线,即大脑半球垂直中线、海马下托内侧面上缘与海马角的外侧缘连线,该软件自动测量得到HIA的角度值。对左右侧HIA均分别测量两次,两次测量时间间隔至少1周,取平均值作为最终结果。由2名具有10年以上胎儿MRI诊断经验,高年资主治医师共同进行这项工作,在影像测量过程中隐藏患者的临床信息。

图1  孕37周胎儿FIESTA序列冠状面脑图像经过脑桥层面勾画HIA的示意图。图中1为海马下托;2为海马角;3为大脑半球垂直中线;4为海马下托内侧面上缘与海马角的外侧缘连线。FIESTA:稳态采集快速成像;HIA:海马折叠角。
Fig. 1  A schematic diagram of HIA is drawn on the coronal brain image of the fetus at 37 weeks of pregnancy using the FIESTA sequence at the pons level. 1 is subiculum; 2 is cornus ammonis; 3 is vertical midline of the cerebral hemisphere; 4 is the line connecting the lateral margin of the cornuammonis with the medial superior margin of the subiculum. FIESTA: fast imaging employing steady state acquisition; HIA: hippocampal infolding angle.

1.4 统计学方法

       使用SPSS 27.0统计软件进行数据处理。正态分布的计量资料采用均数±标准差(x¯±s)表示。对胎儿左右侧HIA值的比较采用配对t检验,对胎儿HIA值的性别比较采用独立样本t检验。将HIA作为因变量、孕龄为自变量进行单因素线性回归分析,获得线性回归方程。P<0.05为差异有统计学意义。

2 结果

2.1 海马折叠角的测量结果

       139例孕中晚期孕妇纳入本研究,年龄18~41(29.76±4.39)岁,孕周(29.17±3.90)周,男胎∶女胎=105∶34。按不同孕周分为6组。对所测得的数据进行分析,获得各组胎儿的HIA值的置信区间(表1),随着孕龄的不断增加,HIA值也在增大;HIA值在20~38周增长了8°~9°。配对t检验分析表明各组胎儿左右两侧HIA值具有显著差异(t=-12.372,P<0.001),且通过HIA的平均值(图2)可以看出各组胎儿右侧HIA大于左侧HIA。HIA值一般在30周之前小于70°(图3)。

图2  不同孕龄左右侧海马折叠角平均值箱式图。
Fig. 2  Box plot of the mean values of hippocampal folding angles on the left and right sides of different gestational age.
图3  不同孕龄FIESTA序列冠状面代表性HIA值。FIESTA:稳态采集快速成像;HIA:海马折叠角。
Fig. 3  Representative HIA values on the coronal plane of FIESTA sequences at different gestational ages. FIESTA: fast imaging employing steady state acquisition; HIA: hippocampal infolding angle.
表1  不同孕龄左右侧HIA的95%置信区间
Tab. 1  95% confidence intervals for the HIA on the left and right sides of different gestational ages

2.2 海马折叠角的性别差异分析

       由于男性胎儿的数量远多于女性胎儿的数量,所以在同孕龄中的男性胎儿中随机抽取与女性胎儿相同数量的样本,组成男胎组(34例)与女胎组(34例),以独立样本t检验分析男性和女性胎儿之间的HIA值,差异无统计学意义(P=0.898),详见表2

表2  男胎与女胎HIA值的比较
Tab. 2  Comparion of HIA values between male and female fetuses

2.3 海马折叠角与孕龄的相关性分析结果

       胎儿左右侧HIA测量结果与孕龄变化的线性回归分析发现,从总体上看,随着孕龄的增加,胎儿左右侧HIA值均呈线性增加的趋势,其与孕龄变化呈正相关关系(R2值分别为左侧0.803、右侧0.836,P均<0.001),详见图4

图4  海马折叠角与孕龄的相关性散点图。4A:左侧海马折叠角;4B:右侧海马折叠角。
Fig. 4  Scatter plot of correlation between hippocampal infolding angle (HIA) and gestational age. 4A: Left HIA; 4B: Right HIA.

3 讨论

       本研究回顾性分析了139例孕妇的资料,在国内首次应用MRI测量获得了20周以后孕中晚期正常在体胎儿HIA数值,并分析其随孕龄变化的发育规律,发现胎儿的HIA值与孕龄呈正相关,随着孕龄的增加而增大,还发现胎儿右侧HIA大于左侧,两侧HIA值之间不存在性别差异。海马是大脑边缘系统的关键结构,在体胎儿MRI图像能够显示正常海马的旋转和发育规律,提供了妊娠中晚期胎儿HIA的精确数据,这些数据为评价胎儿脑发育提供较可靠的参考指标。

3.1 海马折叠角在海马的发育过程中的变化

       本研究发现胎儿的HIA值随着孕龄的增加而增大,两者呈正相关,这与前人的研究结果一致。在人类胚胎发育的过程中,海马发育是其中复杂的环节之一[12, 13]。海马发育始于妊娠8周,于17~18周海马形态开始类似于成年人海马,且在颞叶内侧折叠,随着孕龄增大,海马长轴从几乎垂直的位置逐渐旋转到水平位置,即HIA开始出现角度变化,一般孕25周之前低于70°,孕30周以后高于70°,这种角度值从胚胎期至出生后2年之间增长速度快,而后速度逐渐变缓,并持续到成年[14]

       HIA异常与一些海马结构发育异常的疾病密切相关,如颞叶癫痫、胼胝体发育不良、前脑无裂畸形、海马旋转不良及发育相关肿瘤等[15, 16]。RIGHINI等[7]发现胼胝体发育不良、前脑无裂畸形的病例的HIA测量值较正常胎儿测量值小。KNEZOVIĆ等[17]发现20~35周胼胝体发育不全的胎儿存在海马旋转过程异常,海马体积小,但未进行HIA的测量。此外海马结构和功能的成熟需要多种因素的共同参与。声波刺猬(sonic hedgehog, Shh)信号对于海马体的发育和功能维护非常重要,可调节海马齿状回神经干细胞的分化[18]。HIGASHIJIMA等[19]发现Shh信号相关基因突变所引起的下丘脑错构瘤患者的HIA值较小,推测HIA可能反映了由于异常的Shh信号传导所致颞叶和海马发育不良。因此HIA可以作为宫内或生后评估海马结构发育的有用参数。

3.2 海马折叠角的优势侧及性别差异分析

       本研究发现两侧HIA值不存在性别差异,与之前的文献报道一致[20]。我们的研究还发现孕中晚期胎儿左右两侧HIA值存在半球间差异,OKADA等[14]对儿童及成人HIA测量发现也存在半球间差异,且左侧HIA低于右侧。这与我们的胎儿研究结果比较吻合。但是RIGHINI等和我国学者田路等[21]对孕中晚期在体胎儿和孕中期胎儿标本HIA测量中,并未发现HIA的半球间差异。对于造成两种不同结果的原因尚待推敲。既往文献表明儿童的左右侧前颞叶与海马的体积存在不同,新生儿时期已发现右侧前颞叶及海马结构体积较左侧大,并在出生后的一段时间内差异仍然存在,右侧前颞叶尤为显著[22, 23]。海马体积和HIA的差异是否存在一致性,目前尚无相关的研究。孕中晚期胎儿、儿童和成人的海马发育是否一致,孕期和出生后脑功能的逐渐完善是否会导致半球功能分配的不同,还需要更多产前MRI中心的研究来进一步探讨。

3.3 影响海马发育的因素

       随着科学研究的不断深入,已知多种因素[24, 25]可影响胎儿海马结构的正常发育,并且随着孕妇平均年龄的增高,以及食品、环境等因素的改变,胎儿海马发育异常的概率也在不断增加[26, 27]。海马作为压力调节的关键结构[28],长期焦虑会使血浆中的糖皮质激素分泌过多,导致下丘脑—垂体—肾上腺轴持久亢进,造成海马组织损伤和衰老,海马体积减小[29, 30, 31]。WU等[32]研究了产前孕妇焦虑对胎儿海马早期正常发育的影响,发现产妇怀孕期间焦虑会引起妊娠中末期以及晚期胎儿海马体积减小,左侧海马体较右侧更加明显[33]。这也可能是引起左右侧HIA存在差异的原因,本研究并未排除孕妇焦虑的影响因素,有待进一步的研究。

3.4 本研究的局限性

       本研究存在以下局限性:(1)数据来源于单中心,且样本孕周分布欠均匀,孕21~24周及37~38周胎儿样本量偏少,男性胎儿数量明显多于女性;(2)虽然参照文献规范了HIA测量方法,但手动测量技术可能仍会造成一定人为的误差。

4 结论

       本研究采用MRI测量孕中晚期胎儿的HIA变化数据,发现HIA的增长与孕龄的增加呈正相关,且左右两侧HIA测量值不存在性别差异,但右侧半球的平均HIA测量值大于左侧。这些数据间接反映了正常海马结构的发育规律,对海马发育异常和相关疾病的诊断具有参考意义。

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