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临床研究
3D-IDEAL-IQ定量评估2型糖尿病患者肝脏和胰腺脂肪浸润及其与胰岛素抵抗的相关性
彭晓勇 严俊 黄益龙 王昊雷 何波

Cite this article as: PENG X Y, YAN J, HUANG Y L, et al. Quantitative assessment of liver and pancreatic fat infiltration and its correlation with insulin resistance in type 2 diabetic patients by 3D-IDEAL-IQ[J]. Chin J Magn Reson Imaging, 2023, 14(4): 89-94.本文引用格式:彭晓勇, 严俊, 黄益龙, 等. 3D-IDEAL-IQ定量评估2型糖尿病患者肝脏和胰腺脂肪浸润及其与胰岛素抵抗的相关性[J]. 磁共振成像, 2023, 14(4): 89-94. DOI:10.12015/issn.1674-8034.2023.04.015.


[摘要] 目的 运用3D非对称回波的最小二乘估算法迭代水脂分离(iteraterative decomposition of water and fat with echo asymmetry and least-squares estimation quantitation, IDEAL-IQ)技术定量评估2型糖尿病(type 2 diabetes mellitus, T2DM)患者与健康对照组肝脏和胰腺脂肪浸润含量和分布差异,并对T2DM组肝脏、胰腺脂肪分数(fat fraction, FF)及代谢指标间相关性进行分析。材料与方法 前瞻性招募昆明医科大学第一附属医院经临床确诊的T2DM患者共57例(女25例,男32例),同时招募健康对照组38名(女20例,男18例)。对所有受试者行上腹部MRI扫描,并在MRI检查前一天完成血糖和血脂检测,分别记录两组糖脂代谢指标,计算T2DM组胰岛β细胞分泌指数(homeostasis model assessment of β cell function, HOMA-β)及胰岛素抵抗指数(homeostasis model assessment of insulin resistance, HOMA-IR),进行相关性分析。根据Couinaud分段法将肝脏分为S1~S8段,胰腺则分为胰头、胰体、胰尾三部分。两组间肝脏、胰腺平均FF及肝左叶、右叶FF通过人工分割的方法测量每个肝段及胰腺三部分的FF来计算获得。结果 无论是肝脏、胰腺平均FF还是肝左、右叶及胰腺各部位FF均表现为健康对照组低于T2DM组(P均<0.001),且T2DM组中FF在肝左叶、右叶间及胰腺各部位间差异无统计学意义(P=0.713、0.983);两组间空腹血糖(fasting plasma glucose, FPG)、甘油三酯(triglyceride, TG)、高密度脂蛋白胆固醇(high density lipoprotein cholesterol, HDL-C)差异具有统计学意义(P均<0.001),TG、FPG表现为T2DM组高于健康对照组,而HDL-C则为健康对照组高于T2DM组。T2DM组IR与胰腺平均FF间呈中等正相关。结论 T2DM患者肝脏和胰腺异位脂肪沉积情况可以采用IDEAL-IQ定量技术来评估,且肝脏、胰腺脂肪分布均匀,而HOMA-IR和胰腺平均FF相关。
[Abstract] Objective Quantitative assessment of the differences in the content and distribution of fat infiltration in the liver and pancreas between patients with type 2 diabetes mellitus (T2DM) and healthy controls using the iteraterative decomposition of water and fat with echo asymmetry and least-squares estimation quantitation (3D-IDEAL-IQ) technique, and to analyse the correlation between liver and pancreatic fat fraction (FF) and metabolic indicators in the T2DM group.Materials and Methods A total of 57 clinically diagnosed T2DM patients (25 females and 32 males) were recruited prospectively from the First Affiliated Hospital of Kunming Medical University, while 38 healthy controls (20 females and 18 males) were recruited. Upper abdominal MRI scans were performed on all subjects and glucose and lipid testing was completed one day prior to the MRI examination. The glycolipid metabolic indexes of the two groups were recorded separately, and the pancreatic β-cell secretion index HOMA-β (homeostasis model assessment of β cell function) and insulin resistance index HOMA-IR (homeostasis model assessment of insulin resistance) of the T2DM group were calculated, and the glycolipid metabolic indexes of the two groups were recorded separately for correlation analysis. The liver was divided into S1-S8 segments according to the Couinaud segmentation method, while the pancreas was divided into three parts: the head, body and tail of the pancreas. The mean FF of the liver and pancreas between the two groups and the FF of the left and right lobes of the liver were obtained by measuring the FF of each liver segment and the three parts of the pancreas separately by manual segmentation.Results Both the mean FF in the liver and pancreas and the FF in the left and right lobes of the liver and each part of the pancreas were lower in the healthy control group than in the T2DM group (P<0.001), and the differences in FF in the T2DM group were not statistically significant between the left and right lobes of the liver and between the sites of the pancreas (P=0.713, 0.983). There were statistically significant differences in fasting plasma glucose (FPG), triglyceride (TG) and high-density lipoprotein cholesterol (HDL-C) between the two groups (P<0.001). TG and FPG were higher in the T2DM group than in the healthy control group, while HDL-C were higher in the healthy control group than in the T2DM group. There was a statistical correlation between IR and pancreatic mean FF in the T2DM group, with a moderate positive correlation.Conclusions Ectopic fat deposition in the liver and pancreas of T2DM patients can be assessed using the IDEAL-IQ quantitative technique and the liver and pancreas fat distribution is homogeneous, while HOMA-IR and pancreatic mean FF are correlated.
[关键词] 2型糖尿病;肝脏;胰腺;脂肪定量;磁共振成像
[Keywords] type 2 diabetes mellitus;liver;pancreas;fat quantification;magnetic resonance imaging

彭晓勇 1, 2   严俊 1, 3   黄益龙 1   王昊雷 1   何波 1*  

1 昆明医科大学第一附属医院医学影像科,昆明 650032

2 昆明市儿童医院放射科,昆明 650103

3 曲靖市第一人民医院医学影像科,曲靖 655000

通信作者:何波,E-mail:929883137@qq.com

作者贡献声明:何波设计本研究的方案,对稿件的重要内容进行修改,获得国家自然科学基金项目支持;彭晓勇起草和撰写稿件,获取、分析并解释本研究的数据;严俊、黄益龙参与稿件起草和撰写,获取数据,数据统计分析,对稿件的重要内容进行修改;王昊雷收集、获取及处理数据,参与稿件重要内容修改;全体作者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: 国家自然科学基金 82260338
收稿日期:2022-11-11
接受日期:2023-04-07
中图分类号:R445.2  R587.1 
文献标识码:A
DOI: 10.12015/issn.1674-8034.2023.04.015
本文引用格式:彭晓勇, 严俊, 黄益龙, 等. 3D-IDEAL-IQ定量评估2型糖尿病患者肝脏和胰腺脂肪浸润及其与胰岛素抵抗的相关性[J]. 磁共振成像, 2023, 14(4): 89-94. DOI:10.12015/issn.1674-8034.2023.04.015.

0 前言

       2型糖尿病(type 2 diabetes mellitus, T2DM)是糖尿病最常见的类型。长期脂毒性可导致人体多器官血管和神经损害,影响生活质量。胰岛素抵抗(insulin resistance, IR)是诱发T2DM的重要前驱因素[1, 2, 3],与T2DM患者胰腺、肝脏等器官大量脂肪异位堆积所产生的脂毒性有关[4, 5, 6]。脂肪异位沉积定及分析其与IR的关系具有重要临床意义。目前,病理活检虽然是内脏器官脂肪沉积的“金标准”,但有创且难以综合精确定量是其主要局限。MRI是定量评估肝脏、胰腺脂肪异位沉积的潜在手段。既往学者研究表明,磁共振波谱(magnetic resonance spectroscopy, MRS)能准确测定组织中水与脂肪的比例,被认为是评价肝脏脂质含量的一种参考标准[7]。但仍存在稳定性欠佳、采集时间长、对磁场强度及均匀度要求高等问题。近期有学者利用新兴的非对称回波的最小二乘估算法迭代水脂分离(iteraterative decomposition of water and fat with echo asymmetry and least-squares estimation quantitation, IDEAL-IQ)技术测量胰腺脂肪分数(fat fraction, FF),获得可比拟MRS的准确性[8],且具有成像时间更短、测量方法简单、能将感兴趣区(region of interest, ROI)放置在扫描范围任意位置进行相应区域FF的计算、诊断效能更高的优势[9, 10]。先前国内大多数关于T2DM患者器官脂肪沉积的研究中,同时关注肝脏、胰腺脂肪含量相关性并分析其脂肪含量与临床代谢指标的研究报道较少。部分研究[11, 12, 13]将肝脏、胰腺分别作为单一器官进行分析并探讨了脂肪含量与生化指标的相关性,也有研究[14]仅关注了肝脏、胰腺脂肪沉积,而没有分析与生化指标的相关性。本研究采用3D-IDEAL-IQ技术定量评估T2DM患者肝脏、胰腺脂肪沉积及分布差异,并分析肝脏、胰腺FF及其与胰岛细胞相关代谢指标间的相关性,以期为临床决策及疗效评价提供参考。

1 材料与方法

1.1 一般资料

       本研究为前瞻性研究。招募2019年1月至2023年2月于昆明医科大学第一附属医院经临床确诊的T2DM患者和健康对照组。T2DM组纳入标准参照2016年美国糖尿病协会诊断标准:空腹血糖(fasting plasma glucose, FPG)≥7.0 mmol/L和/或餐后2 h血糖≥11.1 mmol/L;年龄范围28-65岁;亚洲人。T2DM组排除标准:(1)体内含有金属磁性植入物及患有幽闭恐惧症等MRI检查禁忌证;(2)家族遗传性糖尿病和/或妊娠者;(3)既往存在肝脏、胰腺基础疾病者;(4)依靠生命支持系统的危重症患者;(5)长期营养不良者;(6)长期酗酒者(男性≥30 g/d,女性≥20 g/d);(7)长期服用激素者,如类固醇激素等;(8)长期服用噻唑烷二酮类药物者,如吡格列酮等。所纳入T2DM患者未限制患者病程、身体质量指数(body mass index, BMI)及治疗经过。健康对照组无症状和临床表现,排除标准与T2DM组一致。所有志愿者均是通过宣传海报进行招募,且均是自愿参加本次研究,除免费完成本次上腹部MRI扫描,无额外补贴。本研究遵循《赫尔辛基宣言》,经昆明医科大学第一附属医院伦理委员会批准(2018-L-86),全体受试者均签署知情同意书。

       记录T2DM组和健康对照组年龄、性别、BMI、FPG、甘油三酯(triglyceride, TG)、总胆固醇(total cholesterol, TC)和高密度脂蛋白胆固醇(high density lipoprotein cholesterol, HDL-C)、低密度脂蛋白胆固醇(low density lipoprotein cholesterol, LDL-C),并记录T2DM组空腹胰岛素(fasting insulin, FIns)。根据FPG、FIns计算T2DM组胰岛素抵抗指数(homeostasis model assessment of insulin resistance, HOMA-IR)=(FPG×FIns)/22.5;胰岛β细胞分泌指数(homeostasis model assessment of β cell function, HOMA-β)=(20×FIns)/(FPG-3.5)。

1.2 仪器与方法

       检查设备为美国GE 3.0 T(Discovery 750W)MRI仪,采用16通道体部相控阵线圈对所有受试者进行上腹部扫描,采用呼吸门控技术,同时使用腹带加压来减少伪影。检查序列包括:T2WI压脂、轴位IDEAL-IQ、可变容积加速肝脏采集(liver acquisition with volume acceleration flex, LAVA Flex)水脂分离T1WI、3D T1WI、二维快速平衡稳态进动(2D fast imaging employing steady state acquisition, 2D FIESTA),相关扫描参数见表1。所有受试者均在MRI检查前一天完成血脂和血糖检测。

表1  上腹部扫描方案参数
Tab. 1  Parameters of upper abdominal scanning scheme

1.3 图像分析及测量

       肝脏、胰腺FF的计算:在ADW 4.6(GE,美国)后处理工作站上导入所有受试者上腹部MRI图像,选取扫描后自动计算并校正后生成的FF图像,完成肝脏、胰腺FF的ROI勾画(图1、2)。根据Couinaud分段法,肝脏分为S1~S8共八段,在避开胆管、大血管前提下,由两名工作年限分别为5年、2年的住院医师对每个肝段进行三个不同位置ROI勾画,ROI大小均在(200±20)mm²之间,取平均值,将S1段划入肝右叶,记录肝右叶、左叶及肝脏平均FF值。根据解剖分区胰腺分为三部分,即胰头部、体部、尾部,测量方法大致同肝段,ROI大小均在(80±10)mm²之间,记录胰腺各部位及胰腺平均FF值。

图1  肝段脂肪分数感兴趣区(ROI)勾画示意图,ROI 1~8分别对应肝S1~S8段。
图2  胰头、胰体、胰尾各部位脂肪分数ROI勾画示意图,1~3分别对应胰腺头、体、尾部。
Fig. 1  Schematic diagram of of region of interest (ROI) for liver segment fat fraction, ROI 1-8 corresponds to liver S1-S8 respectively.
Fig. 2  ROI sketch map of fat fraction in the head, body and tail of pancreas, ROI 1-3 corresponds to the head, body and tail of pancreas respectively.

1.4 统计学分析

       数据统计学分析处理使用SPSS 25.0软件,计量资料服从正态分布以均数±标准差(x¯±s)来表示,不服从正态分布以中位数(上下四分位数)表示,资料服从正态分布采用独立样本t检验,不服从正态分布则采用曼-惠特尼U检验,等级资料采用秩和检验。服从正态分布采用Pearson相关性分析,不服从正态分布或者等级资料使用Spearman相关性分析。P<0.05被认为差异有统计学意义。

2 结果

2.1 一般资料

       共计95名研究对象被纳入本研究,T2DM患者57例(女25例,男32例),健康对照组38例(女20例,男18例),两组间年龄和性别差异均无统计学意义(P>0.05)。受试者一般资料详见表2

表2  T2DM组和健康对照组一般资料
Tab. 2  General data of T2DM group and healthy control group

2.2 两组间糖脂代谢指标差异比较

       除TC、LDL-C在两组间差异无统计学意义(P>0.05)外,其他指标(HDL-C、TG、FPG)差异均具有统计学意义,T2DM组TG、FPG高于健康对照组,而HDL-C则是健康对照组相对较高(P<0.05)。详见表3

表3  T2DM组与健康对照组糖、脂代谢指标对比
Tab. 3  Comparison of glucose and lipid metabolism indexes between T2DM group and healthy control group

2.3 两组间肝脏、胰腺各部位脂肪含量及分布比较

       两观察者间肝脏FF、胰腺FF一致性检验见表4。T2DM组不仅肝脏、胰腺平均FF高于健康对照组(P均<0.001),且在肝左叶、右叶及胰腺头、体、尾各部位FF均高于健康对照组(P均<0.001);肝右叶、肝左叶间FF及胰腺头、体、尾部间FF在T2DM组中差异无统计学意义(P>0.05);详见表5。同时T2DM组中肝脏平均FF与胰腺平均FF间无显著相关性(r=0.257,P>0.05)。

表4  观察者间一致性检验
Tab. 4  Inter-observer agreement test
表5  T2DM组、健康对照组肝脏及胰腺各部位间FF比较
Tab. 5  Comparison of FF between liver and pancreas in T2DM group and healthy control group

2.4 FF值与各项临床代谢指标间相关性分析

       仅胰腺平均FF与HOMA-IR呈中度正相关(r=0.474,P<0.001,图3),肝脏、胰腺FF与TC、LDL-C、HDL-C、TG、FPG、HOMA-β间及肝脏FF与HOMA-IR均无显著相关性(P均>0.05)。

图3  T2DM组胰腺平均FF与HOMA-IR相关性散点图。T2DM:2型糖尿病;FF:脂肪分数;HOMA-IR:胰岛素抵抗指数。
Fig. 3  Scatter plot of correlation between mean pancreatic FF and HOMA-IR in T2DM group. T2DM: type 2 diabetes mellitus; FF: fat fraction; HOMA-IR: homeostasis model assessment of insulin resistance.

3 讨论

       本研究采用3D-IDEAL-IQ技术对T2DM患者及健康对照组的肝脏、胰腺脂肪含量进行定量评估,并分析T2DM患者肝脏及胰腺FF与临床代谢指标间的关系。研究结果表明T2DM患者肝脏、胰腺FF明显高于健康对照组,但是脂肪沉积在肝脏和胰腺中趋于均匀分布。在T2DM中,仅胰腺平均FF与HOMA-IR存在中度正相关(r=0.474,P<0.001)。既往研究多为单一内脏(肝脏或胰腺)脂肪沉积或多内脏器官脂肪沉积而忽略器官间脂肪沉积相关性以及不同器官脂肪沉积与临床代谢指标间的关系;但是,研究表明,肝脏和胰腺内脂肪沉积的增加,与T2DM的发病率明显相关[14],因此,多器官脂肪定量评估对T2DM患者的全面评估具有重要的临床意义。本研究定量测量T2DM患者肝脏及胰腺FF,并进一步探讨T2DM患者肝脏、胰腺脂肪沉积与临床代谢指标间的关系,借此辅助临床监测T2DM的严重程度及治疗效果。

3.1 T2DM组与健康对照组肝脏、胰腺FF的差异及相关性

       本研究结果表明,T2DM组肝脏、胰腺平均FF、肝左叶、肝右叶及胰头、胰体、胰尾部FF均高于健康对照组,这与先前多数研究[15, 16, 17]结果一致。但是,WADDELL等[18]的研究表明T2DM组仅肝脏FF高于健康对照组,可能是由于该研究中T2DM患者与非T2DM患者BMI无差异。此外,本研究结果表明,T2DM患者中肝左叶、肝右叶间及胰头、胰体、胰尾部之间FF差异无统计学意义。关于T2DM患者胰腺头、体、尾部之间脂肪含量分布是否均匀,现存争议[17,19],可能由于测量方式不一致所造成;也可能与T2DM患者的生活方式相关。在一项关于T2DM患者生活方式因素与胰腺内脂肪沉积之间的相关性研究中发现,胰腺脂肪沉积与每日进食次数相关,每日两餐比每日三餐的胰腺脂肪沉积更高[20]

       本研究中,T2DM患者肝脏平均FF与胰腺平均FF无显著相关性,与国内外研究结论基本一致[21, 22, 23]。这提示肝脏脂肪沉积与胰腺脂肪沉积可能是两个相对独立的过程,先前研究结果也可能是由于样本量少或初诊患者肝脏、胰腺脂肪沉积的关系尚未凸显所致。但也有学者发现T2DM患者肝脏FF与胰腺FF呈正相关[16, 17,24]。本研究由于T2DM组未限制病程及治疗情况,可能会影响肝脏FF与胰腺FF相关性的结果。

3.2 T2DM组与健康对照组间糖脂代谢指标差异

       相对于健康对照组,T2DM组有相对较高水平的FPG、TG和相对较低水平的HDL-C。糖尿病患者由于血糖升高,胰岛素相对缺乏,产生IR,使游离脂肪酸升高,继而出现脂质代谢紊乱,主要表现为TG、TC、LDL-C升高,而HDL-C降低。

3.3 T2DM组肝脏、胰腺FF与IR及胰岛β细胞功能相关性

       在对HOMA-β及HOMA-IR与FF间进行相关性分析时,得出了与先前研究一致的结果[16,24],即胰腺平均FF与HOMA-IR呈正相关,而肝脏平均FF与HOMA-IR无显著相关性,这与先前报道结果不一致[13,24]。分析原因可能是由于本研究中未对T2DM患者的用药情况进行限制,部分药物可能会对肝脏脂肪沉积产生影响。

       越来越多的证据表明肝脏、胰腺内脂肪沉积与T2DM发生、发展密切相关。当肝脏调节葡萄糖和脂肪代谢受损时,则会导致糖脂代谢紊乱继而引发IR,刺激胰岛β细胞分泌,进而出现代偿性高胰岛素血症,随着病情的进展导致胰岛β细胞功能失调,从而加重T2DM;此外,胰腺内异位脂肪沉积产生的脂毒性也可损害胰岛β细胞功能,促进T2DM的发展,最终形成恶性循环。较多研究证实了T2DM的发生与胰腺脂肪沉积有着较为密切的关系[25, 26, 27]。CHEN等[28]指出,胰腺脂肪含量是糖尿病患者潜在的生物标记物,同时胰腺脂肪含量是胰腺导管腺癌的可能危险因素[29]。传统肝脏、胰腺脂肪测量将ROI放置在肝段、胰腺头、体、尾进行准确测量的方法,近年来有学者提出半自动分割技术较传统法可以在保证测量结果准确的情况下,更加节省时间、客观且便利[30, 31, 32]。脂肪可以均匀沉积或不均匀沉积在胰腺实质。大多数情况下脂肪沉积是广泛分布的,即均匀分布在胰腺各部位;然而也会有局灶性或区域性胰腺脂肪沉积的情况,通常发生在胰头和胰尾部[33, 34]

3.4 局限性及展望

       本研究存在一定局限性:第一,本研究未对T2DM患者的用药情况进行限制,这些药物可能会对研究结果产生一定影响,但这也使得纳入本研究的受试者在T2DM患者中更具有代表性;第二,本研究样本量少,未按病程对T2DM患者进行分层研究,未来仍需增大样本量,对不同病程T2DM的异位脂肪沉积情况进行探究。

4 结论

       综上所述,IDEAL-IQ技术可以用来定量评估T2DM患者肝脏、胰腺脂肪异位沉积情况,且胰腺异位脂肪沉积与IR相关,可用于指导T2DM的临床诊疗。

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