术前免疫炎症指标对肝癌肝切除术患者生存预后的预测价值

doi:10.3877/cma.j.issn.2095-3232.2025.05.008

目的

探讨术前免疫炎症指标对肝细胞癌（肝癌）肝切除术患者生存预后的预测价值。

方法

回顾性分析2018年3月至2023年2月在昆明医科大学第二附属医院行肝切除术的232例肝癌患者临床资料。患者均签署知情同意书，符合医学伦理学规定。其中男190例，女42例；年龄33~77岁，中位年龄52岁。采用ROC曲线约登指数法确定中性粒细胞与淋巴细胞比值（NLR）、淋巴细胞与单核细胞比值（LMR）、系统免疫炎症指数（SII）、预后营养指数（PNI）和血红蛋白、白蛋白、淋巴细胞和血小板（HALP）评分的最佳截断值。生存分析采用Kaplan-Meier法和Log-rank检验。采用Cox单因素和多因素回归分析确定患者的生存预后独立影响因素，并构建预后指数（PI）预测模型，ROC曲线分析预测模型对患者2年生存情况的预测效能。

结果

随访期间死亡90例，存活142例；肝癌患者术后1、3、5年生存率分别为93.5%、79.3%、56.5%。NLR、LMR、SII、PNI和HALP评分的最佳截断值分别为2.38、3.53、429.89、347.44、32.64。高NLR组患者术后1、3年生存率分别为82.1%、38.3%，低NLR组相应为89.6%、68.1%；高LMR组的1、3年生存率分别为92.0%、69.0%，低LMR组相应为80.0%、41.2%；高SII组的1、3年生存率分别为84.6%、37.9%，低SII组相应为92.2%、67.9%；高PNI组的1、3年生存率分别为94.0%、75.4%，低PNI组相应为89.4%、44.2%；高HALP组1、3年生存率分别为93.1%、70.6%，低HALP组相应为60.5%、5.0%，以上组间差异均有统计学意义（χ²=16.103，23.882，19.502，23.059，109.681；P<0.001）。Cox单因素和多因素回归分析显示，微血管侵犯、活化部分凝血活酶时间、PNI、HALP评分是患者预后独立影响因素（HR=1.667，0.955，0.997，0.987；P<0.05）。基于独立预后因素构建PI模型，该预测模型的ROC曲线下面积为0.654。

结论

术前NLR、LMR、SII、PNI和HALP评分等免疫炎症指标对肝癌肝切除患者术后生存具有预测作用，基于免疫炎症指标构建的PI模型对生存预后有一定的预测价值。

关键词: 癌，肝细胞, 肝切除术, 淋巴细胞, 血小板, 预后

Objective

To evaluate the predictive value of preoperative inflammatory immune indexes for survival and prognosis of patients with hepatocellular carcinoma (HCC) undergoing hepatectomy.

Methods

Clinical data of 232 HCC patients who underwent hepatectomy in the Second Affiliated Hospital of Kunming Medical University from March 2018 to February 2023 were retrospectively analyzed. The informed consents of all patients were obtained and the local ethical committee approval was received. Among them, 190 patients were male and 42 female, aged from 33 to 77 years, with a median age of 52 years. The optimal cut-off values of neutrophil-lymphocyte ratio (NLR), lymphocyte-monocyte ratio (LMR), systemic immune-inflammation index (SII), prognostic nutritional index (PNI) and hemoglobin, albumin, lymphocyte and platelet (HALP) scores were determined by using the ROC curve and Youden's index. Kaplan-Meier method and Log-rank test were used for survival analysis. Univariate and multivariate Cox's regression analyses were adopted to determine the independent risk factors of patients' survival and prognosis. A prediction model for prognostic index (PI) was constructed. The ROC curve was employed to analyze the prediction efficiency for 2-year overall survival of this prediction model.

Results

During postoperative follow-up, 90 patients died and 142 survived. The 1-, 3-, and 5-year survival rates of HCC patients were 93.5%, 79.3% and 56.5%, respectively. The optimal cutoff values of NLR, LMR, SII, PNI and HALP were 2.38, 3.53, 429.89, 347.44 and 32.64, respectively. The 1- and 3-year survival rates of HCC patients in the high NLR group were 82.1% and 38.3%, respectively, and 89.6% and 68.1% in the low NLR group, respectively. The 1- and 3-year survival rates in the high LMR group were 92.0% and 69.0%, and 80.0% and 41.2% in the low LMR group, respectively. The 1- and 3-year survival rates in the high SII group were 84.6% and 37.9%, and 92.2% and 67.9% in the low SII group, respectively. The 1- and 3-year survival rates in the high PNI group were 94.0% and 75.4%, and 89.4% and 44.2% in the low PNI group, respectively. The 1- and 3-year survival rates in the high HALP group were 93.1% and 70.6%, and 60.5% and 5.0% in the low HALP group, respectively. The differences in these indexes were statistically significant between two groups (χ²=16.103, 23.882, 19.502, 23.059, 109.681; all P<0.001). Univariate and multivariate Cox's regression analyses showed that microvascular invasion, activated partial thromboplastin time, PNI and HALP were the independent prognostic factors (HR=1.667, 0.955, 0.997, 0.987; all P<0.05). PI model was constructed based on the independent prognostic factors, and the area under the ROC curve of the prediction model was 0.654.

Conclusions

Preoperative inflammatory immune indexes, such as NLR, LMR, SII, PNI and HALP, can predict postoperative survival of HCC patients after hepatectomy. PI model based on inflammatory immune indexes has certain predictive value for survival and prognosis.

Key words: Carcinoma, hepatocellular, Hepatectomy, Lymphocyte, Platelet, Prognosis

图1 肝癌患者各指标的ROC曲线注：LMR为淋巴细胞与单核细胞比值，NLR为中性粒细胞与淋巴细胞比值，SII为系统炎症指数，PNI为预后营养指数，HALP评分为血红蛋白、白蛋白、淋巴细胞和血小板评分

图2 肝癌患者各免疫炎症指标分组Kaplan-Meier生存曲线注：LMR为淋巴细胞与单核细胞比值，NLR为中性粒细胞与淋巴细胞比值，SII为系统炎症指数，PNI为预后营养指数，HALP评分为血红蛋白、白蛋白、淋巴细胞和血小板评分

表1 肝癌患者术后预后因素的Cox单因素分析

变量	b	SE(b)	Wald χ²	HR	95% CI	P值
性别	-0.550	0.265	4.609	0.577	0.349~0.953	0.032
年龄	0.018	0.011	2.543	1.018	0.996~1.040	0.111
乙肝	-0.136	0.252	0.289	0.873	0.533~1.431	0.591
肝硬化	0.235	0.242	0.945	1.265	0.788~2.032	0.331
低/未分级	0.525	0.245	4.582	1.691	1.045~2.735	0.032
MVI	0.673	0.215	9.762	1.960	1.285~2.989	0.002
肿瘤直径≥5 cm	-0.104	0.215	0.236	0.901	0.591~1.372	0.627
ALT(U/L)	-0.010	0.005	4.223	0.991	0.982~1.000	0.040
AST(U/L)	0.001	0.003	0.203	1.001	0.995~1.007	0.652
TB(μmol/L)	-0.002	0.013	0.038	0.998	0.973~1.022	0.845
PT(s)	-0.051	0.089	0.338	0.950	0.798~1.130	0.561
APTT(s)	-0.060	0.022	7.668	0.942	0.903~0.983	0.006
AFP(μg/L)	0.316	0.246	1.645	1.371	0.846~2.221	0.200
NLR	0.196	0.045	18.806	1.216	1.113~1.329	<0.001
LMR	-0.204	0.066	9.624	0.815	0.716~0.928	0.002
SII	0.001	0.000	20.442	1.001	1.000~1.001	<0.001
PNI	-0.004	0.001	24.410	0.996	0.994~0.997	<0.001
HALP评分	-0.025	0.005	28.916	0.976	0.967~0.984	<0.001

表1 肝癌患者术后预后因素的Cox单因素分析

变量	b	SE(b)	Wald χ²	HR	95% CI	P值
性别	-0.550	0.265	4.609	0.577	0.349~0.953	0.032
年龄	0.018	0.011	2.543	1.018	0.996~1.040	0.111
乙肝	-0.136	0.252	0.289	0.873	0.533~1.431	0.591
肝硬化	0.235	0.242	0.945	1.265	0.788~2.032	0.331
低/未分级	0.525	0.245	4.582	1.691	1.045~2.735	0.032
MVI	0.673	0.215	9.762	1.960	1.285~2.989	0.002
肿瘤直径≥5 cm	-0.104	0.215	0.236	0.901	0.591~1.372	0.627
ALT(U/L)	-0.010	0.005	4.223	0.991	0.982~1.000	0.040
AST(U/L)	0.001	0.003	0.203	1.001	0.995~1.007	0.652
TB(μmol/L)	-0.002	0.013	0.038	0.998	0.973~1.022	0.845
PT(s)	-0.051	0.089	0.338	0.950	0.798~1.130	0.561
APTT(s)	-0.060	0.022	7.668	0.942	0.903~0.983	0.006
AFP(μg/L)	0.316	0.246	1.645	1.371	0.846~2.221	0.200
NLR	0.196	0.045	18.806	1.216	1.113~1.329	<0.001
LMR	-0.204	0.066	9.624	0.815	0.716~0.928	0.002
SII	0.001	0.000	20.442	1.001	1.000~1.001	<0.001
PNI	-0.004	0.001	24.410	0.996	0.994~0.997	<0.001
HALP评分	-0.025	0.005	28.916	0.976	0.967~0.984	<0.001

表2 肝癌患者术后预后因素的Cox多因素分析

变量	b	SE(b)	Wald χ²	HR	95% CI	P值
MVI	0.511	0.231	4.911	1.667	1.061~2.619	0.027
APTT(s)	-0.046	0.021	4.719	0.955	0.917~0.996	0.030
PNI	-0.003	0.001	6.300	0.997	0.994~0.999	0.012
HALP评分	-0.013	0.006	4.652	0.987	0.975~0.999	0.031

表2 肝癌患者术后预后因素的Cox多因素分析

变量	b	SE(b)	Wald χ²	HR	95% CI	P值
MVI	0.511	0.231	4.911	1.667	1.061~2.619	0.027
APTT(s)	-0.046	0.021	4.719	0.955	0.917~0.996	0.030
PNI	-0.003	0.001	6.300	0.997	0.994~0.999	0.012
HALP评分	-0.013	0.006	4.652	0.987	0.975~0.999	0.031

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Predictive value of preoperative inflammatory immune indexes for survival and prognosis of patients with hepatocellular carcinoma after hepatectomy

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Predictive value of preoperative inflammatory immune indexes for survival and prognosis of patients with hepatocellular carcinoma after hepatectomy