基于HALP评分的列线图模型对肝细胞癌患者肝切除术后预后的预测价值

刘卓然; 黎靖; 周宇; 熊平福; 杨粒; 付文广

doi:10.3969/j.issn.1001-5256.2023.07.014

基于HALP评分的列线图模型对肝细胞癌患者肝切除术后预后的预测价值

DOI: 10.3969/j.issn.1001-5256.2023.07.014

刘卓然^a,
黎靖^a,
周宇^a,
熊平福^a,
杨粒^a,
付文广^{a, b, , ,}

a.
西南医科大学附属医院普通外科(肝胆方向)，四川泸州 646000
b.
西南医科大学附属医院四川省院士(专家)工作站，四川泸州 646000

基金项目:

湖北陈孝平科技发展基金会 (CXPJJH11900001-2019339)

伦理学声明：本研究方案于2022年10月26日经由西南医科大学附属医院伦理委员会审批，批号：KY2022309，所纳入患者均签署知情同意书。

利益冲突声明：本文不存在任何利益冲突。

作者贡献声明：刘卓然、杨粒负责撰写论文；黎靖对研究思路有关键贡献；周宇参加资料的整理分析；熊平福参与修改文章关键内容；付文广指导论文写作。

详细信息

通信作者:
付文广，fuwg@swmu.edu.cn (ORCID：0000-0003-3672-9728)

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出版历程
- 收稿日期: 2022-10-31
- 录用日期: 2022-12-28
- 出版日期: 2023-07-20

Value of the nomogram based on HALP score in predicting the prognosis of patients with hepatocellular carcinoma after hepatectomy

Zhuoran LIU^a,
Jing LI^a,
Yu ZHOU^a,
Pingfu XIONG^a,
Li YANG^a,
Wenguang FU^{a, b
, ,
,}

a.
Department of General Surgery (Hepatobiliary Surgery), The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan 646000, China
b.
Academician (Expert) Workstation of Sichuan Province, The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan 646000, China

Research funding:

Chen Xiao-Ping for the Development of Science and Technology of Hubei Province (CXPJJH11900001-2019339)

More Information

Corresponding author: FU Wenguang, fuwg@swmu.edu.cn (ORCID: 0000-0003-3672-9728)

摘要

摘要: 目的探讨HALP评分在肝细胞癌(HCC)患者肝切除术后预后评估中的应用价值，分析基于HALP评分的列线图模型能否有效预测患者术后生存情况。方法回顾性分析2013年7月—2020年3月在西南医科大学附属医院肝胆外科手术治疗的253例HCC患者临床资料。通过绘制ROC曲线，计算出HALP和其他有关指标的最佳截断值。采用χ²检验分析HALP与临床病理特征之间的关系。使用Kaplan-Meier方法绘制生存曲线，并采用Log-rank检验进行比较。进行单因素分析和多因素Cox回归模型，分析HALP及其他临床参数与患者预后的关系。通过R 3.6软件构建列线图，使用C指数及校准图评价列线图的预测能力，通过净重新分类指数(NRI)、综合判别改善指数(IDI)比较列线图模型和传统模型的预测能力。结果 Kaplan-Meier分析显示高HALP组患者OS、RFS优于低HALP组，差异均有统计学意义(P值均＜0.001)。单因素Cox回归分析显示WBC、GGT、ALP、AFP、手术方式、微血管侵犯、TNM分期、分化程度、HALP、AST/ALT、NLR、MLR均与总生存期(OS)显著相关(P值均＜0.05)，将单因素Cox回归分析中有统计学意义的变量纳入多因素Cox回归分析，结果显示HALP、AST/ALT、ALP、AFP、分化程度、TNM分期是HCC患者术后OS的独立影响因素(P值均＜0.05)。单因素Cox回归分析显示GGT、ALP、AFP、微血管侵犯、TNM分期、分化程度、HALP、AST/ALT、NLR、MLR均与无复发生存期(RFS)显著相关(P值均＜0.05)；多因素Cox回归分析，结果显示HALP、AST/ALT、NLR、ALP、AFP、TNM分期是HCC患者术后RFS的独立影响因素(P值均＜0.05)。根据多因素分析结果分别构建HCC患者OS、RFS的列线图，计算预测OS列线图的C指数为0.732(0.691~0.774)，预测1、3、5年生存率的AUC分别为0.795、0.791、0.775。预测RFS列线图的C指数为0.677(0.637~0.717)，预测1、3、5年生存率的AUC分别为0.742、0.733、0.716；并且1、3、5年OS、RFS校准图表现出了较好的拟合度。结论术前低水平HALP是接受手术治疗的HCC患者长期预后不佳的预测因素，基于HALP评分的列线图模型优于BCLC分期模型，可以更好地预测HCC的预后情况。
- 癌, 肝细胞 /
- 预后 /
- 危险因素 /
- 列线图
Abstract: Objective To investigate the value of HALP score in evaluating the prognosis of patients with hepatocellular carcinoma (HCC) after hepatectomy and whether the nomogram based on HALP score could effectively predict the postoperative survival of patients. Methods A retrospective study was performed for the clinical data of 253 HCC patients who underwent surgical treatment in Department of Hepatobiliary Surgery, The Affiliated Hospital of Southwest Medical University, from July 2013 to March 2020. The receiver operating characteristic (ROC) curve was plotted to calculate the optimal cut-off values of HALP score and other related indicators; the chi-square test was used to investigate the association between HALP score and clinicopathological features; the Kaplan-Meier method was used to plot survival curves, and the Log-rank test method was used for comparison. The univariate and multivariate Cox regression analyses were used to investigate the association of HALP score and other clinical parameters with the prognosis of patients. R3.6 was used to establish a nomogram; C-index and calibration curve were used to evaluate the predictive ability of the nomogram, and net reclassification index (NRI) and integrated discrimination improvement (IDI) were used to compare predictive ability between the nomogram model and the conventional model. Results The Kaplan-Meier analysis showed that the high HALP group had significantly better overall survival (OS) and recurrence-free survival (RFS) than the low HALP group (P < 0.001). The univariate Cox regression analysis showed that white blood cell count, gamma-glutamyl transpeptidase (GGT), alkaline phosphatase (ALP), alpha-fetoprotein (AFP), surgical approach, microvascular invasion, TNM stage, degree of tumor differentiation, HALP, aspartate aminotransferase (AST)/alanine aminotransferase (ALT) ratio, neutrophil-to-lymphocyte ratio (NLR), and monocyte-to-lymphocyte ratio (MLR) were significantly associated with OS (all P < 0.05). The variables with statistical significance in the univariate Cox regression analysis were included in the multivariate Cox regression analysis, and the results showed that ALP, AST/ALT ratio, ALP, AFP, degree of tumor differentiation, and TNM stage were independent influencing factors for OS after surgery in HCC patients (all P < 0.05). The univariate Cox regression analysis showed that GGT, ALP, AFP, microvascular invasion, TNM stage, degree of tumor differentiation, HALP, AST/ALT ratio, NLR, and MLR were significantly associated with RFS (all P < 0.05), and the multivariate Cox regression analysis showed that HALP, AST/ALT ratio, NLR, ALP, AFP, and TNM stage were independent influencing factors for RFS after surgery in HCC patients (all P < 0.05). The nomograms for OS and RFS of HCC patients were established based on the multivariate analysis. The nomogram for OS had a C-index of 0.732 (95% confidence interval [CI]: 0.691-0.774) and an area under the ROC curve of 0.795, 0.791, and 0.775, respectively, in predicting 1-, 3-, and 5-year survival rates, and the nomogram for RFS had a C-index of 0.677 (95%CI: 0.637-0.717) and an area under the ROC curve of 0.742, 0.733, and 0.716, respectively, in predicting 1-, 3-, and 5-year survival rates. The calibration curves of 1-, 3-, and 5-year OS were well fitted to those of 1-, 3-, and 5-year RFS. Conclusion A low level of HALP before surgery is a predictive factor for poor long-term prognosis in HCC patients undergoing surgical treatment, and the nomogram model based on HALP score is superior to the BCLC staging model and can better predict the prognosis of HCC.
- Carcinoma, Hepatocellular /
- Prognosis /
- Risk Factors /
- Nomograms

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图 1 HALP与Alb、LYM、Hb、PLT的ROC曲线

Figure 1. ROC curves of HALP, PLT, LYM, Hb, Alb

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图 2 HCC患者术前HALP水平与OS的生存分析

Figure 2. Survival analysis of HCC patients with preoperative HALP and OS

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图 3 HCC患者术前HALP水平与RFS的生存分析

Figure 3. Survival analysis of HCC patients with preoperative HALP and RFS

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图 4 HCC患者OS列线图模型

Figure 4. Nomogram model for OS in HCC patients

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图 5 HCC患者RFS列线图模型

Figure 5. Nomogram model for RFS in HCC patients

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图 6 预测1、3、5年OS的校准图

Figure 6. Calibration plots for predicting 1 -, 3 -, and 5-year OS

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图 7 预测1、3、5年RFS的校准图

Figure 7. Calibration plots for predicting 1 -, 3 -, and 5-year RFS

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表 1 MLR、NLR、AST/ALT、HALP的诊断指标

Table 1. Diagnostic indicators for MLR, NLR, AST/ALT, HALP

变量	约登指数	截断值	AUC(95%CI)	特异度	敏感度
MLR	0.283	0.39	0.663(0.597~0.729)	0.457	0.826
NLR	0.325	2.92	0.681(0.616~0.746)	0.551	0.774
AST/ALT	0.279	1.02	0.664(0.597~0.730)	0.670	0.609
HALP	0.331	53.22	0.704(0.640~0.767)	0.688	0.643

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表 2 HCC患者的临床病理特征和HALP评分的关系

Table 2. Relationship between clinicopathological characteristics and HALP score of HCC patients

临床特征	低HALP组 (n=136)	高HALP组 (n=117)	χ²值	P值
性别(例)			3.326	0.068
男	111	105
女	25	12
年龄(例)			0.656	0.418
＜60岁	107	87
≥60岁	29	30
TBil(例)			0.168	0.682
＜23 μmol/L	112	94
≥23 μmol/L	24	23
WBC(例)			0.731	0.393
＜10×10⁹/L	124	110
≥10×10⁹/L	12	7
APTT(例)			0.380	0.538
＜35 s	48	37
≥35 s	88	80
GGT(例)			3.132	0.077
＜60 U/L	49	55
≥60 U/L	87	62
ALP(例)			2.925	0.087
＜125 U/L	94	92
≥125 U/L	42	25
AFP(例)			2.308	0.129
＜400 ng/mL	78	78
≥400 ng/mL	58	39
肿瘤大小(例)			19.834	＜0.001
≤5 cm	49	75
＞5 cm	87	42
TNM分期(例)			2.878	0.090
Ⅰ+Ⅱ	121	111
Ⅲ+Ⅳ	15	6
分化程度(例)			4.160	0.041
低	28	13
中+高	108	104
手术方式(例)			8.846	0.003
开腹	124	91
腹腔镜	12	26
微血管侵犯(例)			0.127	0.721
无	102	90
有	34	27
HBsAg(例)			2.027	0.155
阴性	18	9
阳性	118	108
BCLC分期(例)			1.301	0.254
0+A	91	86
B+C	45	31

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表 3 HCC患者OS的单因素和多因素分析

Table 3. Univariate and multivariate analysis of OS in HCC patients

临床特征	单因素分析		多因素分析
临床特征	HR(95%CI)	P值	HR(95%CI)	P值
性别(男/女)	1.125(0.713~1.775)	0.612
年龄(＜60岁/≥60岁)	0.809(0.537~1.219)	0.312
TBil(23 μmol/L/≥23 μmol/L)	1.247(0.832~1.869)	0.286
WBC(＜10×10⁹/L/≥10×10⁹/L)	1.801(1.052~3.084)	0.032
APTT(＜35 s/≥35 s)	1.047(0.733~1.495)	0.800
GGT(＜60 U/L/≥60 U/L)	1.552(1.095~2.201)	0.014
ALP(＜125 U/L/≥125 U/L)	2.015(1.421~2.857)	＜0.001	1.502(1.017~2.221)	0.041
AFP(＜400 ng/mL/≥400 ng/mL)	2.328(1.665~3.253)	＜0.001	2.128(1.499~3.020)	＜0.001
手术方式(开腹/腔镜)	0.519(0.299~0.902)	0.020
术后住院时间(＜12 d/≥12 d)	1.374(0.976~1.934)	0.069
HBsAg(阴性/阳性)	1.020(0.597~1.745)	0.941
微血管侵犯(无/有)	1.479(1.010~2.167)	0.045
TNM分期(Ⅰ+Ⅱ/Ⅲ+Ⅳ)	3.745(2.256~6.217)	＜0.001	2.346(1.318~4.175)	0.004
分化程度(低/中+高)	0.525(0.349~0.787)	0.002	0.643(0.418~0.990)	0.045
HALP(＜53.22/≥53.22)	0.395(0.275~0.567)	＜0.001	0.555(0.373~0.827)	0.004
AST/ALT(＜1.02/≥1.02)	1.827(1.297~2.572)	0.001	1.585(1.101~2.282)	0.013
NLR(＜2.92/≥2.92)	2.561(1.827~3.590)	＜0.001
MLR(＜0.39/≥0.39)	2.148(1.535~3.005)	＜0.001

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表 4 HCC患者RFS的单因素和多因素分析

Table 4. Univariate and multivariate analysis of RFS in HCC patients

临床特征	单因素分析		多因素分析
临床特征	HR(95%CI)	P值	HR(95%CI)	P值
性别(男/女)	0.830(0.535~1.287)	0.404
年龄(＜60岁/≥60岁)	0.896(0.627~1.279)	0.544
TBil(23 μmol/L/≥23 μmol/L)	1.140(0.787~1.651)	0.489
WBC(＜10×10⁹/L/≥10×10⁹/L)	1.601(0.955~2.683)	0.074
APTT(＜35 s/≥35 s)	1.242(0.899~1.716)	0.189
GGT(＜60 U/L/≥60 U/L)	1.433(1.054~1.947)	0.022
ALP(＜125 U/L /≥125 U/L)	1.930(1.403~2.653)	＜0.001	1.535(1.070~2.202)	0.020
AFP(＜400 ng/mL/≥400 ng/mL)	1.630(1.207~2.201)	0.001	1.498(1.101~2.038)	0.010
手术方式(开腹/腔镜)	0.672(0.426~1.060)	0.087
术后住院时间(＜12 d/≥12 d)	1.105(0.819~1.492)	0.513
HBsAg(阴性/阳性)	0.955(0.605~1.507)	0.842
微血管侵犯(无/有)	1.510(1.074~2.121)	0.018
TNM分期(Ⅰ+Ⅱ/Ⅲ+Ⅳ)	2.839(1.732~4.656)	＜0.001	1.919(1.107~3.325)	0.020
分化程度(低/中+高)	0.652(0.446~0.953)	0.027
HALP(＜53.22/≥53.22)	0.568(0.419~0.771)	＜0.001	0.704(0.503~0.985)	0.041
AST/ALT(＜1.02/≥1.02)	1.465(1.087~1.974)	0.012	1.378(1.004~1.891)	0.047
NLR(＜2.92/≥2.92)	1.955(1.451~2.634)	＜0.001	1.476(1.014~2.150)	0.042
MLR(＜0.39/≥0.39)	1.696(1.253~2.296)	0.001

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表 5 列线图与BCLC分期的预测价值比较

Table 5. Comparison of the predictive value of nomograms with BCLC staging

模型	NRI(95%CI)	P值	IDI(95%CI)	P值
BCLC分期	Reference		Reference
OS列线图	0.307(0.101~0.515)	＜0.000 1	0.307(0.139~0.415)	＜0.000 1
RFS列线图	0.754(0.557~0.885)	＜0.000 1	0.700(0.548~0.788)	＜0.000 1

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