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World Journal of Gastroenterology
世界胃肠病学杂志

Comparative study of indocyanine green-R15, Child-Pugh score, and model for end-stage liver disease score for prediction of hepatic encephalopathy after transjugular intrahepatic portosystemic shunt
吲哚菁绿-R15、Child-Pugh 评分和终末期肝病评分模型在预测经颈静脉肝内门体分流术后肝性脑病方面的比较研究

Zhong Wang, Yi-Fan Wu, Zhen-Dong Yue, Hong-Wei Zhao, Lei Wang, Zhen-Hua Fan, Yu Zhang, Fu-Quan Liu
Zhong Wang、Yi-Fan Wu、Zhen-Dong Yue、Hong-Wei Zhao、Lei Wang、Zhen-Hua Fan、Yu Zhang、Fu-Quan Liu

ORCID number: Zhong Wang 00000003-3575-1982; Yi-Fan Wu 00000003-2709-2729; Zhen-Dong Yue 0000-0001-5403-8336; Hong-Wei Zhao 0000-0001-5657-1839; Lei Wang 0000-0003-4080-1630; ZhenHua Fan 0000-0001-5417-1997; Yu Zhang 0000-0001-9895-175X; FuQuan Liu 0000-0003-1972-7712.
Author contributions: Liu FQ designed the research; Zhang , Wu YF, Yue ZD, Zhao HW, Wang , and Fan ZH performed the research; Wang analyzed the data and wrote the paper.
ORCID 编号:王中 00000003-3575-1982;吴一凡 00000003-2709-2729;岳振东 0000-0001-5403-8336;赵宏伟 0000-0001-5657-1839;王磊 0000-0003-4080-1630;范振华 0000-0001-5417-1997;张宇 0000-0001-9895-175X;刘福全 0000-0003-1972-7712。作者贡献刘福全设计了该研究;张 、吴 YF、岳 ZD、赵 HW、王 和范 ZH 执行了该研究;王 分析了数据并撰写了论文。

Supported by Beijing Municipal Science and Technology
北京市科学技术委员会资助
Commision, No. 委员会,No.
Z181100001718097.

Institutional review board
机构审查委员会

statement: The study was reviewed and approved by the Institutional Review Board of Shijitan Hospital, Capital Medical University.

Conflict-of-interest statement:
利益冲突声明:

There are no conflicts of interest related to this study.
本研究不涉及任何利益冲突。

Data sharing statement: No
数据共享声明:无

additional data are available.
Open-Access: This article is an open-access article that was
开放获取:本文是一篇开放获取的文章。

Zhong Wang, Yi-Fan Wu, Zhen-Dong Yue, Hong-Wei Zhao, Lei Wang, Zhen-Hua Fan, Yu Zhang, FuQuan Liu, Department of Interventional Therapy, Beijing Shijitan Hospital, Capital Medical University, Beijing 100038, China
首都医科大学附属北京世纪坛医院介入治疗科 王中、吴一凡、岳振东、赵宏伟、王磊、范振华、张宇、刘福全,北京 100038
Corresponding author: Fu-Quan Liu, BCPS, MD, Director, Professor, Department of Interventional Therapy, Beijing Shijitan Hospital, Capital Medical University, No. 10 Tie Yi Road, Yangfangdian, Haidian District, Beijing 100038, China. lfuquan@aliyun.com
通讯作者刘福全,BCPS,医学博士,首都医科大学附属北京世纪坛医院介入治疗科主任、教授,地址:北京市海淀区羊坊店铁一路10号,邮编:100038。lfuquan@aliyun.com。

Abstract 摘要

BACKGROUND 背 景

Hepatic encephalopathy (HE) remains an enormous challenge in patients who undergo transjugular intrahepatic portosystemic shunt (TIPS) implantation. The preoperative indocyanine green retention rate at (ICG-R15), as one of the liver function assessment tools, has been developed as a prognostic indicator in patients undergoing surgery, but there are limited data on its role in TIPS.
肝性脑病(HE)仍然是经颈静脉肝内门体分流术(TIPS)植入患者面临的巨大挑战。作为肝功能评估工具之一,术前吲哚青绿在 (ICG-R15)的滞留率已被开发为手术患者的预后指标,但有关其在 TIPS 中作用的数据却很有限。

AIM

To determine whether the ICG-R15 can be used for prediction of post-TIPS HE in decompensated cirrhosis patients with portal hypertension (PHT) and compare the clinical value of ICG-R15, Child-Pugh score (CPS), and model for end-stage liver disease (MELD) score in predicting post-TIPS HE with PHT.
目的:确定 ICG-R15 是否可用于预测门脉高压症(PHT)失代偿期肝硬化患者的 TIPS 后高血压,并比较 ICG-R15、Child-Pugh 评分(CPS)和终末期肝病模型(MELD)评分在预测 PHT 患者 TIPS 后高血压方面的临床价值。

METHODS 方法

This retrospective study included 195 patients with PHT who underwent elective TIPS at Beijing Shijitan Hospital from January 2018 to June 2019. All patients underwent the ICG-R15 test, CPS evaluation, and MELD scoring before TIPS. According to whether they developed HE or not, the patients were divided into two groups: HE group and non-HE group. The prediction of one-year postTIPS HE by ICG-R15, CPS and MELD score was evaluated by the areas under the receiver operating characteristic curves (AUCs).
这项回顾性研究纳入了2018年1月至2019年6月在北京世纪坛医院接受择期TIPS治疗的195例PHT患者。所有患者在TIPS前均接受了ICG-R15检测、CPS评估和MELD评分 。根据是否发生 HE,将患者分为两组:HE 组和非 HE 组。通过接收器操作特征曲线下面积(AUCs)评估 ICG-R15、CPS 和 MELD 评分对 TIPS 术后一年 HE 的预测。

RESULTS 结果

A total of 195 patients with portal hypertension were included and 23% (45/195) of the patients developed post-TIPS HE. The ICG-R15 was identified as an independent predictor of post-TIPS HE. The AUCs for the ICG-R15, CPS, and MELD score for predicting post-TIPS HE were 0.664 ( confidence interval [CI]:
共纳入 195 名门脉高压患者,其中 23% 的患者(45/195)出现了 TIPS 后高血压。ICG-R15被确定为TIPS后高血压的独立预测因子。ICG-R15、CPS和MELD评分预测TIPS后高血压的AUC为0.664( 置信区间 [CI]:

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Manuscript source: Unsolicited manuscript
稿件来源未经请求的手稿
Specialty type: Gastroenterology and hepatology
专科类型:肠胃病学和肝病学

Country/Territory of origin: China
原产国/地区:中国

Peer-review report's scientific
同行评审报告的科学性

quality classification
Grade A (Excellent): A
A 级(优秀):A
Grade B (Very good): B, B
B 级(很好):B、B
Grade C (Good): 0
C 级(良好):0
Grade D (Fair): 0
D 级(尚可):0
Grade E (Poor): 0
E 级(差):0

Received: November 23, 2020
收到:2020 年 11 月 23 日

Peer-review started: November 23 , 2020
同行评审开始:2020 年 11 月 23 日
First decision: December 17, 2020
首次决定2020 年 12 月 17 日
Revised: December 20, 2020
修订:2020 年 12 月 20 日
Accepted: January 15, 2021
接受:2021 年 1 月 15 日
Article in press: January 15, 2021
文章已付印:2021 年 1 月 15 日
Published online: February 7, 2021
在线出版:在线发布:2021 年 2 月 7 日
P-Reviewer: Joko K, Liem S,
P-评审员Joko K, Liem S、
Martins VH 马丁斯 VH
S-Editor: Fan JR S 编辑Fan JR
L-Editor: Wang TQ L 编辑Wang TQ
P-Editor: Wang LL (95%CI: , and 0.641 (95%CI: ), respectively. The non-parametric approach (DelongDelong & Clarke-Pearson) showed that there was statistical significance in pairwise comparison between AUCs of ICG-R15 and MELD score .
P 编辑: (95%CI: , 和 0.641 (95%CI: )。非参数方法(DelongDelong & Clarke-Pearson)显示,ICG-R15 的 AUC 与 MELD 评分 成对比较具有统计学意义。

CONCLUSION 结 论

The ICG-R15 has appreciated clinical value for predicting the occurrence of postTIPS HE and is a choice for evaluating the prognosis of patients undergoing TIPS.
ICG-R15 在预测 TIPS 后 HE 的发生方面具有令人赞赏的临床价值,是评估 TIPS 患者预后的一种选择。
Key Words: Hepatic encephalopathy; Indocyanine green-R15; Child-Pugh score; Model for end-stage liver disease score; Transjugular intrahepatic portosystemic shunt; Portal hypertention
关键字肝性脑病;吲哚菁绿-R15;Child-Pugh 评分;终末期肝病评分模型;经颈静脉肝内门体分流术;门脉高压症
CThe Author(s) 2021. Published by Baishideng Publishing Group Inc. All rights reserved.
作者:2021.白石登出版集团公司出版。保留所有权利。
Core Tip: We studied whether the indocyanine green retention rate at (ICGR15) can be used for prediction of post-transjugular intrahepatic portosystemic shunt (TIPS) hepatic encephalopathy (HE) in decompensated cirrhosis patients with portal hypertension (PHT) and compare the clinical value of ICG-R15, Child-Pugh score, and model for end-stage liver disease score in predicting post-TIPS HE with PHT.
核心提示我们研究了吲哚青绿在 (ICGR15)的滞留率是否可用于预测门脉高压症(PHT)失代偿期肝硬化患者经颈静脉肝内门体分流术(TIPS)后肝性脑病(HE),并比较了 ICG-R15、Child-Pugh 评分和终末期肝病评分模型在预测门脉高压症 TIPS 后 HE 中的临床价值。
Citation: Wang Z, Wu YF, Yue ZD, Zhao HW, Wang L, Fan ZH, Zhang Y, Liu FQ. Comparative study of indocyanine green-R15, Child-Pugh score, and model for end-stage liver disease score for prediction of hepatic encephalopathy after transjugular intrahepatic portosystemic shunt. World J Gastroenterol 2021; 27(5): 416-427
引用:Wang Z, Wu YF, Yue ZD, Zhao HW, Wang L, Fan ZH, Zhang Y, Liu FQ.吲哚菁绿-R15、Child-Pugh评分和终末期肝病评分模型预测经颈静脉肝内门体分流术后肝性脑病的比较研究。World J Gastroenterol 2021; 27(5):416-427

INTRODUCTION 引言

Portal hypertension (PHT) is a very common and serious complication of chronic liver disease that often causes variceal bleeding and refractory ascites . Transjugular intrahepatic portosystemic shunt (TIPS) is an important treatment option that has been shown to be efficacious in the management of . This procedure can alleviate portal hypertension by creating a large channel between the portal vein and hepatic vein . Unfortunately, TIPS can cause severe complications such as heart failure, liver failure, and hepatic encephalopathy (HE). HE has a high incidence rate and is one of the most debilitating complications, which has a serious effect on the prognosis and survival of patients . Although some risk factors are known, the identification of patients at risk of HE needs additional research. It is important to predict post-TIPS HE so that prevention and treatment measures can be implemented in high-risk HE patients to avoid adverse outcomes.
门静脉高压症(PHT)是慢性肝病的一种非常常见且严重的并发症,通常会导致静脉曲张出血和难治性腹水 。经颈静脉肝内门体分流术(TIPS)是一种重要的治疗方法,已被证明对治疗 具有疗效。这种手术可在门静脉和肝静脉之间建立一个大通道,从而缓解门静脉高压 。遗憾的是,TIPS 可引起严重并发症,如心力衰竭、肝功能衰竭和肝性脑病(HE)。肝性脑病的发病率很高,是最令人衰弱的并发症之一,严重影响患者的预后和存活率 。尽管已知一些风险因素,但如何识别有 HE 风险的患者仍需进一步研究。预测 TIPS 后高血压非常重要,这样才能对高危高血压患者采取预防和治疗措施,避免不良后果。
The indocyanine green retention rate at (ICG-R15), the Child-Pugh score (CPS), and the model for end-stage liver disease (MELD) score have been developed to assess liver function . The ICG-R15 is a relatively non-invasive, quick, and inexpensive method that has been widely used in patients with end-stage liver disease . Zipprich et reported that ICG is the most accurate predictor among quantitative liver function tests of the survival of patients with cirrhosis . A recent retrospective study demonstrated that preoperative ICG clearance was predictive of the surgical prognosis in patients undergoing hepatectomy . The CPS was developed to assess the severity of liver cirrhosis in the clinic. This scoring system includes the bilirubin level, the albumin level, the prothrombin time, HE, and ascites . The MELD score is used to predict the survival of patients undergoing TIPS and to evaluate patients with severe liver disease prior to transplantation. It includes three objective variables: The total bilirubin level, the creatinine level, and the international normalized ratio (INR) . However, there are limited data on the use of liver function tools, especially the ICG-R15, to predict post-TIPS HE. Therefore, the aim of this study was to compare the clinical value of the MELD score, CPS, and ICG-R15 for the prediction of post-TIPS HE in patients with PHT.
(ICG-R15)、Child-Pugh 评分 (CPS) 和终末期肝病模型 (MELD) 评分已被开发用于评估肝功能 。ICG-R15 是一种相对无创、快速、廉价的方法,已广泛应用于终末期肝病患者 。Zipprich 等 报道,在肝硬化患者生存率的定量肝功能检测中,ICG 是最准确的预测指标 。最近的一项回顾性研究表明,术前 ICG 清除率可预测肝切除术患者的手术预后 。CPS 是为在临床上评估肝硬化的严重程度而开发的。该评分系统包括胆红素水平、白蛋白水平、凝血酶原时间、HE 和腹水 。MELD 评分用于预测接受 TIPS 患者的存活率,并在移植前对严重肝病患者进行评估。它包括三个客观变量:总胆红素水平、肌酐水平和国际标准化比值(INR) 。然而,使用肝功能工具(尤其是 ICG-R15)预测 TIPS 后 HE 的数据有限。因此,本研究旨在比较 MELD 评分、CPS 和 ICG-R15 对预测 PHT 患者 TIPS 后 HE 的临床价值。

MATERIALS AND METHODS 材料和方法

This retrospective study was approved by the Ethics Committee of Beijing Shijitan Hospital of Capital Medical University. The need to obtain informed consent was waived due to its retrospective nature.
这项回顾性研究获得了首都医科大学附属北京世纪坛医院伦理委员会的批准。由于该研究具有回顾性,因此无需获得知情同意。

Patients 患者

All patients who underwent TIPS between January 2018 and June 2019 in the interventional department of Beijing Shijitan Hospital were included in this study.
本研究纳入了2018年1月至2019年6月期间在北京世纪坛医院介入科接受TIPS治疗的所有患者。
The following inclusion criteria were set: (1) Patients between 18 and 70 years old; (2) Patients diagnosed with PHT; and (3) Patients who underwent TIPS using a polytetrafluoroethylene-covered stent. The following exclusion criteria were set: (1) Preoperative HE; (2) Liver cancer; (3) Liver transplantation; (4) TIPS retreatment; (5) Non-cirrhotic PHT; (6) Surgical splenectomy; (7) Portal vein thrombosis; and (8) Urgent TIPS.
纳入标准如下:(1) 年龄在 18 至 70 岁之间的患者;(2) 确诊为 PHT 的患者;(3) 使用聚四氟乙烯支架接受 TIPS 的患者。排除标准如下:(1) 术前高血压;(2) 肝癌;(3) 肝移植;(4) TIPS 再治疗;(5) 非肝硬化性 PHT;(6) 外科脾切除术;(7) 门静脉血栓形成;(8) 急诊 TIPS。

Definitions 定义

PHT was defined as the radiological presence of significant splenomegaly, umbilical vein recanalization, and/or portosystemic shunts as well as a preoperative platelet count . Portal pressure gradient values greater than or equal to indicated clinically significant .
PHT 的定义是:在放射学上存在明显的脾肿大、脐静脉再通和/或门体分流,以及术前血小板计数 。门静脉压力梯度值大于或等于 表示具有临床意义
HE was defined as neuropsychiatric abnormalities ranging from mild neuropsychological dysfunction to deep coma and abnormal ammonia levels, after the exclusion of other possible causes of altered mental status by computed tomography or magnetic resonance imaging .
HE 被定义为通过计算机断层扫描或磁共振成像 排除其他可能导致精神状态改变的原因后,出现从轻度神经心理功能障碍到深度昏迷和氨水平异常的神经精神异常。

Preoperative ICG-R15, CPS, and MELD score
术前 ICG-R15、CPS 和 MELD 评分

All patients included in this study underwent the ICG-R15 test with a dyedensitogram (DDG) analyser (Japan, NIHON KOHDEN, model DDG-3300K) and an ICG clearance rate test (Japan, NIHON KOHDEN, model A). Within after the injection of ICG into the median cubital vein, plasma ICG concentrations were monitored via a sensor attached to the patients' finger. The ICG-R15 was subsequently assessed by a computer. The CPS score can be divided into three grades depending on the total points: Grade A (5-6 points), B (7-9 points), and C points). The MELD score was calculated based on the following formula: (bilirubin creatinine aetiology (biliary and alcoholic 0 , others 1 (Figure 1).
本研究中的所有患者均使用染色密度图(DDG)分析仪(日本,NIHON KOHDEN,型号 DDG-3300K)进行了 ICG-R15 试验,并进行了 ICG 清除率试验(日本,NIHON KOHDEN,型号 A)。向患者肘正中静脉注射 ICG 后,在 内通过连接在患者手指上的传感器监测血浆 ICG 浓度。随后由计算机对 ICG-R15 进行评估。CPS 评分根据总分可分为三个等级:A 级(5-6 分)、B 级(7-9 分)和 C 级 分)。MELD 评分根据以下公式计算: (胆红素 肌酐 病因(胆汁性和酒精性 0 ,其他 1 (图 1)。

TIPS 提示

Under fluoroscopic guidance, a standard TIPS procedure was performed by an experienced interventional radiologist. A pigtail catheter was inserted into the right internal jugular vein leading to the hepatic veins. After finding the portal vein through the superior mesenteric artery or splenic artery using indirect portal venography, a stent , or , Fluency, Bard, United States) was placed to create a channel between the hepatic vein and the portal vein. Afterward, the portal vein pressure was measured at least three times, and a pressure transducer system (Combitrans, Braun Melsungen, Germany) with a multichannel monitor (Sirecust, Siemens, Germany) was used to measure the haemodynamic parameters.
在透视引导下,经验丰富的介入放射科医生进行了标准的 TIPS 手术。将一根尾纤导管插入通往肝静脉的右颈内静脉。利用间接门静脉造影术通过肠系膜上动脉或脾动脉找到门静脉后,放置支架 ,或 ,Fluency,Bard,United States),在肝静脉和门静脉之间建立通道。之后,测量门静脉压力至少三次,并使用带有多通道监视器(Sirecust,德国西门子公司)的压力传感器系统(Combitrans,德国博朗梅尔松根公司)测量血流动力学参数。

Statistical analysis 统计分析

Clinical and laboratory characteristics were collected from the medical records. SPSS (version 20.0, SPSS Inc., United States) and MedCalc were used for the statistical analyses. Descriptive data are presented as the mean , and qualitative variables are presented as frequencies or percentages. Student's test or the Mann-Whitney test was used to compare quantitative variables between groups, and the chi-square test or Fisher's exact test was used for qualitative variables. Univariate and multivariable logistic regression analyses were used to determine HE-related risk factors after TIPS. The areas under the receiver operating characteristic curves (AUCs) for the ICG-R15, CPS, and MELD score were evaluated. The non-parametric approach (Delong-Delong & Clarke-Pearson) was used for pairwise comparison among AUCs of ICG-R15, CPS, and MELD score. Statistical significance was established at .
临床和实验室特征均从病历中收集。统计分析采用 SPSS(20.0 版,美国 SPSS 公司)和 MedCalc。描述性数据以平均值 表示,定性变量以频率或百分比表示。组间定量变量的比较采用学生 检验或 Mann-Whitney 检验,定性变量的比较采用卡方检验或费雪精确检验。单变量和多变量逻辑回归分析用于确定TIPS术后与高血压相关的风险因素。评估了 ICG-R15、CPS 和 MELD 评分的接收器操作特征曲线下面积(AUC)。采用非参数方法(Delong-Delong & Clarke-Pearson) 对 ICG-R15、CPS 和 MELD 评分的 AUCs 进行配对比较。统计显著性以 为标准。
Figure 1 Receive operating characteristic curve analyses of indocyanine green-R15, Child-Pugh score, and model for end-stage liver disease score to predict post-transjugular intrahepatic portosystemic shunt hepatic encephalopathy. ICG: Indocyanine green; MELD: Model for end-stage liver disease.
图 1 预测经颈静脉肝内门体系统分流术后肝性脑病的吲哚菁绿-R15、Child-Pugh 评分和终末期肝病模型评分的接受操作特征曲线分析。ICG:吲哚菁绿;MELD:终末期肝病模型。

RESULTS 结果

Patients' preoperative characteristics
患者术前特征

A total of 221 patients who underwent TIPS were included in this study. After applying the inclusion and exclusion criteria of the study, data were collected from a total of 195 decompensated cirrhosis patients with PHT who underwent TIPS. The basic clinical characteristics are listed in Table 1. The study population comprised 140 men and 55 women, with a mean age of years. The indications included variceal bleeding in patients, refractory ascites in , variceal bleeding combined with ascites in ), and other (including pleural fluid and hepatorenal syndrome) in . The most common cause of cirrhosis was viral cirrhosis ( ), followed by alcoholic cirrhosis ( ), biliary cirrhosis ( ), and drug-induced and autoimmune hepatitis cirrhosis (4.6%). According to the CPS, 108 patients were classified as having grade A, 75 as having grade B and 12 as having grade C. The median MELD score and ICG-R15 were and , respectively.
本研究共纳入了221名接受TIPS治疗的患者。在应用研究的纳入和排除标准后,共收集了 195 名接受 TIPS 的 PHT 失代偿期肝硬化患者的数据。基本临床特征见表 1。研究对象包括 140 名男性和 55 名女性,平均年龄为 岁。适应症包括 患者的静脉曲张出血、 患者的难治性腹水、 患者的静脉曲张出血合并腹水以及 患者的其他(包括胸腔积液和肝肾综合征)。最常见的肝硬化病因是病毒性肝硬化( ),其次是酒精性肝硬化( )、胆汁性肝硬化( )以及药物性和自身免疫性肝炎肝硬化(4.6%)。根据 CPS,108 名患者被划分为 A 级,75 名为 B 级,12 名为 C 级。MELD 评分和 ICG-R15 的中位数分别为

Univariable and multivariable analyses of post-TIPS HE
TIPS 后 HE 的单变量和多变量分析

Of the 195 patients who underwent TIPS, 45 (23%) developed HE at the 12 mo followup. The factors associated with HE in univariable analysis included age, stent size, puncture site, ICG-R15, CPS, MELD score, blood urea nitrogen (BUN) level, and level , and 0.044 , respectively). As shown in Table 2, multivariate regression analysis identified the following variables as independent risk factors for post-TIPS HE: Older age, stent size, puncture site in the right branch of the portal vein, high ICG-R15, high BUN level, high level, high CPS, and high MELD score.
在接受 TIPS 的 195 名患者中,有 45 人(23%)在 12 个月的随访中出现了 HE。单变量分析中与 HE 相关的因素包括年龄、支架大小、穿刺部位、ICG-R15、CPS、MELD 评分、血尿素氮(BUN)水平和 ,分别为 0.044 和 0.044)。如表 2 所示,多变量回归分析确定以下变量为 TIPS 后 HE 的独立危险因素:年龄较大、支架大小 、穿刺部位位于门静脉右支、ICG-R15 偏高、BUN 水平偏高、 水平偏高、CPS 偏高和 MELD 评分偏高。

Discriminatory power of the CPS, MELD score, and ICG-R15
CPS、MELD 评分和 ICG-R15 的鉴别力

The area under the receiver operating characteristic (ROC) curve for the ICG-R15 (AUC confidence interval [CI]: ) for the prediction of post-TIPS HE was larger than those of the CPS (AUC CI: ) and the MELD score (AUC CI: . The nonparametric approach (Delong-Delong & Clarke-Pearson) showed that there was no statistical significance in pairwise comparison between AUCs of ICG-R15 and MELD score . The cut-off value for the ICG-R15, which was determined by the maximum of Youden index, was 30 , with a sensitivity of and specificity of for the prediction of post-TIPS HE (Table 3). Of the 126 patients with an ICGR15 > 30, developed post-TIPS HE, while of 69 patients with an ICG developed post-TIPS HE.
ICG-R15 预测 TIPS 后 HE 的接收器操作特征曲线下面积(AUC 置信区间 [CI]: )大于 CPS(AUC CI: )和 MELD 评分(AUC CI: )。非参数方法(Delong-Delong & Clarke-Pearson) 显示,ICG-R15 和 MELD 评分的 AUC 成对比较无统计学意义 。根据尤登指数最大值确定的 ICG-R15 临界值为 30,预测 TIPS 后 HE 的灵敏度为 ,特异度为 (表 3)。在 ICGR15 > 30 的 126 例患者中, 出现了 TIPS 后 HE,而在 ICG 的 69 例患者中, 出现了 TIPS 后 HE。
Table 1 Patients' preoperative characteristics
表 1 患者术前特征
Parameter
Patients enrolled
入选患者
Patients without post-TIPS
无 TIPS 后遗症的患者
HE
Patients with post-TIPS HE
TIPS 后 HE 患者
value
Age (years)
Gender 0.79
TIPS indication,
TIPS 指示、
0.10
Variceal bleeding 静脉曲张出血 93 25
Ascites 29 7
Bleeding combine with ascites
出血合并腹水
21 6
Other 7 7
Cirrhotic aetiology,
肝硬化病因
0.98
Viral 111 35
Alcoholic 25 6
Biliary 7 2
Drug-induced 3 1
Autoimmune 4 1
Preoperative HVPG,
术前 HVPG、
0.28
Preoperative PPG,
术前 PPG、
0.6
Stent size, 0.057
7 51 8
8 87 30
10 12 7
Puncture site of portal vein,
门静脉穿刺部位、
Left branch 96 17
Bifurcation 15 7
Right branch 40 20
Child-Pugh score
儿童普氏评分
Child-Pugh grade,
Child-Pugh 年级、
A 89 19
B 55 20
C 6 6
MELD score 0.07
ICG-R15,
Total protein,  总蛋白质 0.19
Total bilirubin,
总胆红素
0.169
Creatinine, 0.084
0.889
0.442
0.39
Albumin, 0.12
Serum potassium,
血清钾、
0.62
Serum clozapine,
血清氯氮平、
0.81
Serum sodium,  血清钠、 0.39
0.26
Platelet count  血小板计数 0.49
0.9
0.07
0.76
0.50
0.39
0.69

Comparison of post-TIPS-HE incidence between patients with an ICG-R15 and
ICG-R15 和 ICG-R15 患者的 TIPS-HE 后发病率比较

The patients were divided into two groups according to the ICG-R15 cut-off value, , determined by the maximal Youden index. Patients with an ICG-R15 had a higher incidence of HE than those with an ICG-R15<30% (13% vs . There were significant differences in age, CPS, preoperative portal pressure gradient, , albumin, aspartate transaminase, , white blood cells, active partial thromboplastin, or prothrombin time in patients with different ICG-R15 levels below and above (Table 4 ).
根据最大尤登指数确定的 ICG-R15 临界值 ,将患者分为两组。ICG-R15 的患者比 ICG-R15<30% 的患者有更高的 HE 发生率(13% vs 。在 ICG-R15 水平低于和高于 的不同患者中,年龄、CPS、术前门脉压力梯度、 、白蛋白、天冬氨酸转氨酶、 、白细胞、活性部分凝血活酶或凝血酶原时间均存在明显差异(表 4)。

DISCUSSION 讨论

TIPS has been widely used to treat complications of PHT, including varices and ascites, by creating a large channel between the hepatic vein and portal vein. This procedure changes the liver haemodynamics by shunting a fraction of the portal venous blood directly into the systemic circulation, which can lead to decreased liver blood supply and impaired liver function reserve. In addition, HE occurs because of an increase in the amount of natural toxins such as ammonia travelling to the brain as a result of the shunting of the blood directly from the portal vein to the hepatic vein . can produce a spectrum of neurological/psychiatric syndromes ranging from subclinical alterations to coma. It remains one of the most common and worrisome complications of end-stage liver disease after TIPS .
TIPS 通过在肝静脉和门静脉之间建立一个大通道,广泛用于治疗 PHT 的并发症,包括静脉曲张和腹水。这种手术通过将部分门静脉血液直接分流到全身循环来改变肝脏血流动力学,从而导致肝脏供血减少和肝功能储备受损。此外,由于血液从门静脉直接分流到肝静脉,导致流向大脑的天然毒素(如氨)数量增加,也会导致 HE 的发生 ,可产生一系列神经/精神综合征,从亚临床改变到昏迷不等。它仍然是 TIPS 后终末期肝病最常见、最令人担忧的并发症之一
The ICG-R15 test is simple, fast, less invasive, and inexpensive, and can be performed in less than half an hour. The ICG-R15 retention trial was introduced as a relatively noninvasive tool for the classification of pediatric and adult patients with acute and chronic liver failure . A particular advantage of the ICG-R15 test is that it is more suitable for pediatric patients. In addition, the trial appears to be an ideal way to assess the risks of surgical procedures such as liver resection. In addition to assessing the predictive value of varices and ascites, the results of some papers suggest that the ICG-R15 test may also predict mortality .
ICG-R15 试验简单、快速、侵入性小且价格低廉,可在半小时内完成。ICG-R15 留置试验是一种相对无创的工具,用于对急性和慢性肝功能衰竭的儿童和成人患者进行分类 。ICG-R15 试验的一个特别优势是它更适合儿科患者。此外,该试验似乎也是评估肝切除等外科手术风险的理想方法。除了评估静脉曲张和腹水的预测价值外,一些论文的结果表明 ICG-R15 试验还可以预测死亡率
In this study, univariate and multivariate logistic analyses showed that stent size, puncture site in the right branch of the portal vein, age, ICG-R15, BUN level, level, CPS, and MELD score were predictors of post-TIPS HE in patients with portal hypertension. Patients with puncture sites in the right portal vein had a high incidence of post-TIPS HE. This is related to the right branch of the portal vein contains more poisons mainly received from the superior mesenteric vein . It was reported that choosing the left branch of the portal vein as the puncture site during the placement of TIPS may decrease the incidence of HE significantly . HE occurs more often in patients with a stent diameter of than in those with smaller-diameter stents. A
本研究的单变量和多变量逻辑分析表明, 支架大小、穿刺部位位于门静脉右支、年龄、ICG-R15、BUN 水平、 水平、CPS 和 MELD 评分是门静脉高压症患者 TIPS 后 HE 的预测因素。穿刺部位位于右门静脉的患者发生 TIPS 后 HE 的几率很高。这与门静脉右支含有较多主要来自肠系膜上静脉的毒物有关 。据报道,在置入 TIPS 时选择门静脉左支作为穿刺部位可显著降低 HE 的发生率 。与使用小直径支架的患者相比,支架直径为 的患者更常发生 HE。A
Table 2 Univariable and multivariable logistic regression analyses of post-transjugular intrahepatic portosystemic shunt hepatic encephalopathy
表 2 经颈静脉肝内门体系统分流术后肝性脑病的单变量和多变量逻辑回归分析
Parameter Univariable logistic regression
单变量逻辑回归
Multivariable logistic regression
多变量逻辑回归
Regression
coefficient
OR value
Regression
coefficient
OR value
Age 0.53 1.055 0.057 1.059
Gender (F/M) 0.134 1.143 0.789
TIPS indication (variceal
TIPS 适应症(静脉曲张
bleeding/ascites/bleeding combined with
出血/荨麻疹/出血合并
ascites/other) 腹水/其他)
0.147 1.159 0.522
Cirrhotic aetiology 肝硬化病因
(viral/alcoholic/biliary/drug-
(病毒/酒精/胆汁/药物
induced/autoimmune) 诱发/自身免疫)
0.053 0.761 0.437
Preoperative HVPG 术前 HVPG 0.019 1.019 0.502
Preoperative PPG 术前 PPG 0.022 1.023 0.289
Stent size -0.975 0.377
Puncture site of portal vein (left
门静脉穿刺部位(左
branch/bifurcation/right branch)
分支/分叉/右分支)
0.763 2.145 0.566 1.762
Child-Pugh score 儿童普氏评分 0.027 1.027 0.053 1.055
Child-Pugh grade (A/B/C)
Child-Pugh 等级(A/B/C)
0.196 0.594 1.216
MELD score 0.256 1.291 0.516 1.068
ICG-R15 0.026 1.027 0.028 1.029
Total protein 蛋白质总量 -0.029 0.972 0.203
Total bilirubin 总胆红素 0.000 1.000 0.962
Creatinine 0.006 1.006 0.151
ALT 0.000 1.000 0.892
AST 0.003 1.003 0.232
ALP 0.002 1.002 0.248
Albumin -0.058 0.94 0.1364
Serum potassium 血清钾 0.233 1.262 0.689
Serum clozapine 血清氯氮平 0.007 1.007 0.864
Serum sodium -0.035 0.965 0.395
WBC 0.047 1.049 0.544
Platelet count 血小板计数 -0.003 0.997 0.359
-0.001 0.999 0.908
BUN 0.084 1.087 0.085 1.008
0.025 1.025 0.032 1.033
APTT -0.015 0.985 0.768
INR -0.644 0.525 0.504
FIB 0.248 1.281 0.389
PT -0.059 0.943 0.559
.
. TIPS: Transjugular intrahepatic portosystemic shunt; HVPG: Hepatic venous pressure gradient; PPG: Portal pressure gradient; MELD: Model for end-stage liver disease; ICG: Indocyanine green; ALT: Alanine aminotransferase; AST: Aspartate transaminase; ALP: Alkaline phosphatase; Hb: Hemoglobin; BUN: Blood urea nitrogen; APTT: Active partial thromboplastin; INR: International normalized ratio; FIB: Fibrinogen; PT: Prothrombin time; WBC: White blood cell.
.TIPS:HVPG:肝静脉压力梯度;PPG:门静脉压力梯度;MELD:终末期肝病模型;ICG:吲哚菁绿;ALT:丙氨酸氨基转移酶;AST:天门冬氨酸转氨酶;ALP:碱性磷酸酶;Hb:血红蛋白;BUN:血尿素氮;APTT:活性部分凝血活酶;IN:血红蛋白:ALP:碱性磷酸酶;Hb:血红蛋白;BUN:血尿素氮;APTT:活性部分凝血活酶;INR:国际标准化比率;FIB:纤维蛋白原;PT:凝血酶原时间;WBC:白细胞:白细胞
Table 3 Areas under the receiver operating characteristic curves of indocyanine green rentention rate of , Child-Pugh score, and model for end-stage liver disease score
表 3 、Child-Pugh 评分和终末期肝病评分模型的吲哚菁绿染色保留率的接收者操作特征曲线下面积
Parameter CPS MELD ICG-R15
AUC 0.596 0.641 0.664
CI
Z statistic 1.709 2.293 2.832
value 0.087
Youden index J 尤登指数 J 0.211 0.269 0.307
Cut-off value 临界值 6 7.5 30
Sensitivity 78.2 60.87 86.96
Specificity 42.6 66.07 43.75
< 0.01. ICG: Indocyanine green; CPS: Child-Pugh score; MELD: Model for end-stage liver disease; AUS: Areas under the receiver operating characteristic curves.
< 0.01.ICG:吲哚菁绿;CPS:Child-Pugh 评分;MELD:终末期肝病模型;AUS:接收者操作特征曲线下的面积。
Table 4 Characteristics of patients with an indocyanine green rentention rate at and
表 4 和 中吲哚菁绿留存率的患者特征
Characteristic ICG-R15 ICG-R15 > 30%  ICG-R15 > 30 value
non
Age
Child-Pugh score
儿童普氏评分
Preoperative PPG,
术前 PPG、
Albumin,
Serum clozapine,
血清氯氮平、
Serum sodium,  血清钠、
APTT,
PT,
larger stent can effectively reduce portal vein pressure, but at the same time, more blood that has not been detoxified by the liver directly enters the systemic circulation, which can further impair liver function and lead to HE. However, some studies showed that the incidence of post-TIPS HE was unrelated to stent diameter . Li et al also found that age and Child-Pugh classification were independent risk factors for early post-TIPS , which was in accord with previous studies . Fonio et al demonstrated that the MELD grade was a risk factor for post-TIPS HE; the results of this study support this finding . Normally, ammonia is detoxified by conversion to urea by Krebs-Henseleit buffer or the urea cycle in the liver. In total, to of the urea nitrogen in the primary urine is absorbed in the renal tubules and collecting tubes. A high incidence of HE was found in patients with high BUN levels, which is related to the aggravation of liver function involving the kidneys, renal decompensation, and azotaemia .
较大的支架可以有效降低门静脉压力,但同时会有更多未经肝脏解毒的血液直接进入全身循环,从而进一步损害肝功能并导致 HE。然而,一些研究表明,TIPS 后 HE 的发生率与支架直径无关 。Li 等 也发现年龄和 Child-Pugh 分级是早期 TIPS 后 的独立风险因素,这与之前的研究 一致。Fonio 等 证实,MELD 分级是 TIPS 后 HE 的风险因素;本研究结果支持这一发现 。正常情况下,氨通过克雷布斯-亨斯莱特缓冲液或肝脏中的尿素循环转化为尿素进行解毒。 的尿素氮被肾小管和集合管吸收。在高 BUN 水平的患者中,高尿酸血症的发病率很高,这与涉及肾脏的肝功能恶化、肾功能失代偿和氮质血症有关
Hiwatashi found that a higher ICG-R15 was significantly correlated with surgical complications and liver dysfunction after surgical resection and chemotherapy in patients with colorectal cancer . Wang et al demonstrated that the ICG-R15 could more accurately predict preoperative liver reserve function than the Child-Pugh and MELD scores in patients who suffered from liver cancer . Another study showed that the ALICE scoring system (including serum albumin and ICG-R15) could simply and effectively predict the prognosis of liver cancer patients undergoing surgery . In this study, we analysed and compared the areas under the ROC curves for the ICG-R15, CPS, and MELD score. The results were as follows: , and there was statistical significance in pairwise comparison between AUCs of ICG-R15 and MELD score. This suggests that the ICG-R15 has clinical equivalent value to predict post-TIPS HE compared to MELD score. The CPS is relatively restricted because it includes two subjective variables (HE and severity of ascites , and the limited values ranging from 5 to 15 make it imprecise. The boundary values for the five parameters were chosen empirically and have not been formally validated . In some situations, the predictive value of MELD may be reduced. Malabsorption of vitamin K secondary to cholestasis can cause an increase in the INR; starvation and infection can increase the level of bilirubin; and the use of diuretics can increase the level of creatinine . As a quantitative assessment, the ICGR15 is a simple and practical way to assess liver function and is widely used in patients undergoing liver surgery. The ICG-R15 may play a role in predicting postTIPS HE; consequently, it may be useful for identifying high-risk patients.
Hiwatashi 发现,ICG-R15 较高与结直肠癌患者手术切除和化疗后的手术并发症和肝功能异常显著相关 。Wang 等人 证实,在肝癌患者中,ICG-R15 比 Child-Pugh 和 MELD 评分更能准确预测术前肝储备功能 。另一项研究表明,ALICE 评分系统(包括血清白蛋白和 ICG-R15)可简单有效地预测接受手术的肝癌患者的预后 。在本研究中,我们分析并比较了 ICG-R15、CPS 和 MELD 评分的 ROC 曲线下面积。结果如下: ICG-R15 和 MELD 评分的 AUC 成对比较具有统计学意义。这表明,与 MELD 评分相比,ICG-R15 在预测 TIPS 后 HE 方面具有同等的临床价值。由于 CPS 包括两个主观变量(HE 和腹水严重程度 ),且其数值范围有限,从 5 到 15 不等,因此限制相对较多。五个参数的边界值是根据经验选择的,尚未经过正式验证 。在某些情况下,MELD 的预测价值可能会降低。继发于胆汁淤积的维生素 K 吸收不良可导致 INR 升高;饥饿和感染可使胆红素水平升高;使用利尿剂可使肌酐水平升高 。作为一种定量评估,ICGR15 是一种简单实用的肝功能评估方法,被广泛用于肝脏手术患者。ICG-R15 可在预测TIPS 后 HE 方面发挥作用,因此可用于识别高风险患者。
The optimal ICG-R15 cut-off value in our study was , and it divided the patients into two groups with different risks of post-TIPS HE. This difference was highly significant , which implies that TIPS patients with an ICG-R15 should be given special care during perioperative management. However, we did not compare the role of the CPS, MELD score, and ICG-R15 for predicting the survival of patients after TIPS, which needs further study. In addition, future studies should analyse the incidence of complications and survival between different ICG-R15 groups. A small number of patients with Child-Pugh C cirrhosis and the low median MELD score were limitations of this study. Since this may be related to the small sample size, we will increase the amount of the sample in the future.
在我们的研究中,ICG-R15 的最佳临界值为 ,它将患者分为两组,两组患者发生 TIPS 后 HE 的风险不同。这一差异非常明显 ,这意味着ICG-R15 的TIPS患者在围手术期管理中应给予特殊照顾。但是,我们没有比较 CPS、MELD 评分和 ICG-R15 在预测 TIPS 患者生存率方面的作用,这需要进一步研究。此外,未来的研究还应该分析不同 ICG-R15 组别的并发症发生率和存活率。本研究的局限性在于Child-Pugh C肝硬化患者人数较少以及MELD评分中位数较低。由于这可能与样本量较小有关,我们将在今后增加样本量。
In summary, the ICG-R15 can be used for predicting post-TIPS HE in patients with PHT. We propose using the ICG-R15 to evaluate the risk of HE in PHT patients undergoing TIPS.
总之,ICG-R15 可用于预测 PHT 患者 TIPS 后的 HE。我们建议使用 ICG-R15 评估接受 TIPS 的 PHT 患者发生 HE 的风险。

CONCLUSION 结 论

TIPS for PHT in patients with cirrhosis should be considered after careful selection based on patient characteristics and liver function. The ICG-R15 has appreciated clinical value for predicting the occurrence of post-TIPS HE and is a choice for evaluating the prognosis of patients undergoing TIPS.
肝硬化患者在接受TIPS治疗PHT时,应根据患者特征和肝功能进行慎重选择。ICG-R15 对预测 TIPS 后 HE 的发生具有重要的临床价值,是评估 TIPS 患者预后的一种选择。

ARTICLE HIGHLIGHTS 文章要点

Research background 研究背景

Transjugular intrahepatic portosystemic shunt (TIPS) is a technique for the treatment of portal hypertension-related complications such as esophageal variceal bleeding and refractory ascites by establishing shunt channels in the hepatic parenchyma between the hepatic vein and the portal vein. It can also be used as a bridging therapy for decompensated patients with cirrhosis and other patients waiting for liver transplantation. However, the high incidence of postoperative hepatic encephalopathy (HE) seriously affects the prognosis and survival of patients, and it is particularly important to find accurate methods to predict post-TIPS HE. Some studies have shown that the clearance rate of indocyanine green before operation has good predictive value for the prognosis of patients undergoing hepatectomy. We hypothesized that indocyanine green retention rate at (ICG-R15) may can predict postoperative HE after TIPS (post-TIPS HE); therefore, prevention and treatment can be implemented in high-risk HE patients to avoid adverse outcomes.
经颈静脉肝内门体分流术(TIPS)是一种通过在肝静脉和门静脉之间的肝实质内建立分流通道,治疗食管静脉曲张出血和难治性腹水等门静脉高压相关并发症的技术。它还可用作肝硬化失代偿期患者和其他等待肝移植患者的桥接疗法。然而,术后肝性脑病(HE)的高发生率严重影响了患者的预后和生存,因此,找到预测TIPS术后HE的准确方法尤为重要。有研究表明,术前吲哚菁绿的清除率对肝切除术患者的预后有很好的预测价值。我们假设吲哚青绿在 (ICG-R15)的滞留率可以预测 TIPS 术后 HE(TIPS 术后 HE),因此可以对高风险 HE 患者进行预防和治疗,避免不良后果的发生。

Research motivation 研究动机

TIPS is currently used in the management of complications of portal hypertension.
TIPS 目前用于门脉高压并发症的治疗。
However, the incidence of HE remains an issue in TIPS placement and affects patient quality of life and long-term outcomes. The preoperative ICG-R15 has been developed as a prognostic indicator in patients undergoing surgery, but there are limited data on its role in TIPS. The purpose of this study was to explore whether ICG-R15 can be used as a predictor of post-TIPS HE and compared the clinical value of the ICG-R15, ChildPugh score (CPS), and model for end-stage liver disease (MELD) score for the prediction of post-TIPS HE in decompensated cirrhosis patients with portal hypertension (PHT).
然而,高血压的发生率仍是 TIPS 置管术中的一个问题,并影响患者的生活质量和长期预后。术前 ICG-R15 已被开发为手术患者的预后指标,但有关其在 TIPS 中作用的数据有限。本研究旨在探讨 ICG-R15 是否可用作 TIPS 术后 HE 的预测指标,并比较 ICG-R15、ChildPugh 评分(CPS)和终末期肝病模型(MELD)评分在预测门脉高压症(PHT)失代偿期肝硬化患者 TIPS 术后 HE 的临床价值。

Research objectives 研究目标

The aim of this study was to explore whether ICG-R15 can be used as a predictor of post-TIPS HE and compared the clinical value of the ICG-R15, CPS, and MELD score for the prediction of post-TIPS HE in decompensated cirrhosis patients with PHT. According to the ICG-R15 value, appropriate and timely intervention can be implemented in patients with high-risk HE patients.
本研究旨在探讨ICG-R15是否可作为TIPS后高血压的预测指标,并比较ICG-R15、CPS和MELD评分在预测PHT失代偿期肝硬化患者TIPS后高血压方面的临床价值。根据 ICG-R15 值,可以对高危 HE 患者实施适当和及时的干预。

Research methods 研究方法

We conducted a prospective study of 195 patients with PHT who underwent elective TIPS. All patients underwent the ICG-R15 test, CPS evaluation, and MELD scoring. According to whether they developed HE or not, the patients were divided into two groups: HE group and non-HE group. Descriptive data are presented as the mean , and qualitative variables are presented as frequencies or percentages. Student's test or the Mann-Whitney test was utilized to compare quantitative variables between groups, and the chi-square test or Fisher's exact test was used for qualitative variables. Univariate and multivariable logistic regression analyses were used to determine HE-related risk factors after TIPS. The prediction of one-year post-TIPS HE by ICG-R15, CPS, and MELD score was evaluated by the areas under the receiver operating characteristic curves (AUCs). Pairwise comparison of AUCs in three different function tools was analysed.
我们对 195 名接受择期 TIPS 的 PHT 患者进行了前瞻性研究。所有患者均接受了 ICG-R15 测试、CPS 评估和 MELD 评分。根据是否发生 HE,患者被分为两组:HE 组和非 HE 组。描述性数据以平均值 表示,定性变量以频率或百分比表示。组间定量变量的比较采用学生 检验或 Mann-Whitney 检验,定性变量的比较采用卡方检验或费雪精确检验。采用单变量和多变量逻辑回归分析来确定 TIPS 术后与 HE 相关的风险因素。通过接收器操作特征曲线下面积(AUC)评估了 ICG-R15、CPS 和 MELD 评分对 TIPS 术后一年 HE 的预测。对三种不同功能工具的 AUC 进行了配对比较分析。

Research results 研究成果

A total of 195 patients with PHT were included and 23% (45/195) of the patients developed post-TIPS HE. The ICG-R15 was identified as an independent predictor of post-TIPS HE. The AUCs for the ICG-R15, CPS, and MELD score for predicting postTIPS HE were confidence interval [CI]: (95%CI: ), and 0.641 ( CI: , respectively. Molodianovitch et showed that there was statistical significance in pairwise comparison between AUCs of ICG-R15 and MELD score .
共纳入了 195 名 PHT 患者,其中 23% 的患者(45/195)出现了 TIPS 后 HE。ICG-R15被确定为TIPS后高血压的独立预测因子。ICG-R15、CPS和MELD评分预测TIPS后高血压的AUC分别为 置信区间[CI]: (95%CI: )和0.641( CI: )。Molodianovitch 等人的研究表明 ,ICG-R15 和 MELD 评分的 AUCs 成对比较具有统计学意义

Research conclusions 研究结论

TIPS for PHT in patients with cirrhosis should be considered after careful selection based on patient characteristics and liver function. The ICG-R15 has appreciated clinical value for predicting the occurrence of post-TIPS HE and is a choice for evaluating the prognosis of patients undergoing TIPS.
肝硬化患者在接受TIPS治疗PHT时,应根据患者特征和肝功能进行慎重选择。ICG-R15 对预测 TIPS 后 HE 的发生具有重要的临床价值,是评估 TIPS 患者预后的一种选择。

Research perspectives 研究视角

We can learn from this study that monitoring patients who underwent TIPS with an ICG-R15 value above can better prevent adverse outcomes. Future studies will focus on the incidence of complications and survival in terms of the value of ICG-R15 and randomized controlled trials are needed in order to verify our results.
从本研究中我们可以了解到,对接受 TIPS 的 ICG-R15 值高于 的患者进行监测,可以更好地预防不良后果的发生。今后的研究将重点关注 ICG-R15 值的并发症发生率和存活率,并需要随机对照试验来验证我们的结果。

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  1. Values are the mean .
    数值为平均值 。
    Values are
    数值为
    Values are medians (P25, P75).
    数值为中位数(P25、P75)。
    .
    . TIPS: Transjugular intrahepatic portosystemic shunt; HE: Hepatic encephalopathy; HVPG: Hepatic venous pressure gradient; PPG: Portal pressure gradient; MELD: Model for end-stage liver disease; ICG: Indocyanine green; ALT: Alanine aminotransferase; AST: Aspartate transaminase; ALP: Alkaline phosphatase; Hb: Hemoglobin; BUN: Blood urea nitrogen; APTT: Active partial thromboplastin; INR: International normalized ratio; FIB: Fibrinogen; PT: Prothrombin time; WBC: White blood cells.
    .TIPS:HE:肝性脑病;HVPG:肝静脉压力梯度;PPG:门静脉压力梯度;MELD:终末期肝病模型;ICG:靛青绿;ALT:丙氨酸氨基转移酶;AST:天门冬氨酸氨基转移酶;ALP:碱性磷酸酶;Hb:血红蛋白;BUN:血尿素氮;APTT:活性部分凝血酶原;IN:血红蛋白:ALP:碱性磷酸酶;Hb:血红蛋白;BUN:血尿素氮;APTT:活性部分凝血活酶;INR:国际标准化比率;FIB:纤维蛋白原;PT:凝血酶原时间;WBC:白细胞:白细胞
  2. Values are .
    数值为 。
    Values are the mean .
    数值为平均值 。
    Values are medians (P25, P75).
    数值为中位数(P25、P75)。
    .
    .
    . ICG: Indocyanine green; HE: Hepatic encephalopathy; PPG: Portal pressure gradient; AST: Aspartate transaminase; APTT: Active partial thromboplastin; PT: Prothrombin time; WBC: White blood cells.
    .ICG:吲哚菁绿;HE:肝性脑病;PPG:门静脉压力梯度;AST:天门冬氨酸转氨酶;APTT:活性部分凝血酶原;PT:凝血酶原时间;WBC:白细胞:APTT:活化部分凝血活酶;PT:凝血酶原时间;WBC:白细胞:白细胞