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World Journal of Gastroenterology

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
Commision, No. 委员会,No.

Institutional review board

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

Conflict-of-interest statement:

There are no conflicts of interest related to this study.

Data sharing statement: No

additional data are available.
Open-Access: This article is an open-access article that was

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

Abstract 摘要


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。


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。


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。


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
Specialty type: Gastroenterology and hepatology

Country/Territory of origin: China

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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。


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.
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


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。


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.

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.
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)。


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。


Patients' preoperative characteristics

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
Patients enrolled
Patients without post-TIPS
无 TIPS 后遗症的患者
Patients with post-TIPS HE
TIPS 后 HE 患者
Age (years)
Gender 0.79
TIPS indication,
TIPS 指示、
Variceal bleeding 静脉曲张出血 93 25
Ascites 29 7
Bleeding combine with ascites
21 6
Other 7 7
Cirrhotic aetiology,
Viral 111 35
Alcoholic 25 6
Biliary 7 2
Drug-induced 3 1
Autoimmune 4 1
Preoperative HVPG,
术前 HVPG、
Preoperative PPG,
术前 PPG、
Stent size, 0.057
7 51 8
8 87 30
10 12 7
Puncture site of portal vein,
Left branch 96 17
Bifurcation 15 7
Right branch 40 20
Child-Pugh score
Child-Pugh grade,
Child-Pugh 年级、
A 89 19
B 55 20
C 6 6
MELD score 0.07