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ISSN 1001-5256 (Print)
ISSN 2097-3497 (Online)
CN 22-1108/R

Value of a risk assessment model in predicting venous thromboembolism in patients with liver failure after artificial liver support therapy

DOI: 10.3969/j.issn.1001-5256.2023.03.019
Research funding:

Research funding: National Natural Science Foundation of China (81702011);

Research Project of Modern Hospital Management and Development Institute of Nanjing University and Medical Development and Medical Assistance Fund of Nanjing Drum Tower Hospital (NDYG2021016)

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  • Corresponding author: LU Sufang, sufanglu0708@126.com (ORCID: 0000-0001-5471-2511)
  • Received Date: 2022-08-01
  • Accepted Date: 2022-10-11
  • Published Date: 2023-03-20
  •   Objective  To investigate the value of a risk assessment model in predicting venous thromboembolism (VTE) in patients with liver failure after artificial liver support therapy.   Methods  A retrospective analysis was performed for the clinical data of 124 patients with liver failure who received artificial liver support therapy in Affiliated Drum Tower Hospital of Nanjing University Medical School from March 2019 to December 2021, among whom there were 41 patients with VTE (observation group) and 143 patients without VTE (control group). Related clinical data were compared between the two groups, and the Caprini risk assessment model was used for scoring and risk classification of the patients in both groups. The t-test was used for comparison of continuous data between two groups; the chi-square test was used for comparison of categorical data between two groups; the Mann-Whitney U rank sum test was used for comparison of ranked data between two groups. The logistic regression analysis was used to investigate the independent risk factors for VTE in patients with liver failure after artificial liver support therapy. The receiver operating characteristic (ROC) curve was used to investigate the value of Caprini score and the multivariate predictive model used alone or in combination in predicting VTE.  Results  The observation group had a significantly higher Caprini score than the control group (4.39±1.10 vs 3.12±1.04, t=6.805, P < 0.001). There was a significant difference between the two groups in risk classification based on Caprini scale (P < 0.05), and the patients with high risk or extremely high risk accounted for a higher proportion among the patients with VTE. The univariate analysis showed that there were significant differences between the two groups in age (t=6.400, P < 0.001), catheterization method (χ2=14.413, P < 0.001), number of times of artificial liver support therapy (Z=-4.720, P < 0.001), activity (Z=-6.282, P < 0.001), infection (χ2=33.071, P < 0.001), D-dimer (t=8.746, P < 0.001), 28-day mortality rate (χ2=5.524, P=0.022). The multivariate analysis showed that number of times of artificial liver support therapy (X1) (odds ratio [OR]=0.251, 95% confidence interval [CI]: 0.111-0.566, P=0.001), activity (X2) (OR=0.122, 95%CI: 0.056-0.264, P < 0.001), D-dimer (X3) (OR=2.921, 95%CI: 1.114-7.662, P=0.029) were independent risk factors for VTE in patients with liver failure after artificial liver support therapy. The equation for individual predicted probability was P=1/[1+e-(7.425-1.384X1-2.103X2+1.072X3)]. The ROC curve analysis showed that Caprini score had an area under the ROC curve of 0.802 (95%CI: 0.721-0.882, P < 0.001), and the multivariate model had an area under the ROC curve of 0.768 (95%CI: 0.685-0.851, P < 0.001), while the combination of Caprini score and the multivariate model had an area under the ROC curve of 0.957 (95%CI: 0.930-0.984, P < 0.001).  Conclusion  The Caprini risk assessment model has a high predictive efficiency for the risk of VTE in patients with liver failure after artificial liver support therapy, and its combination with the multivariate predictive model can significantly improve the prediction of VTE.

     

  • 肝硬化心肌病(cirrhotic cardiomyopathy,CCM)是肝硬化患者存在特有的循环功能障碍,在静息时常常无任何临床症状,在运动、药物激发、出血和外科手术时会出现心率加快、心输出量增加、外周血管阻力下降、动脉血压降低、心肌收缩/舒张功能降低、对刺激的反应性减弱等心脏功能异常表现,严重者出现心力衰竭或猝死1-2。近来多项研究表明该病症可能与腹水、食管胃底静脉曲张破裂出血、大手术或肝移植后死亡率增加有关。CCM的发病机制仍不明确,目前认为涉及心肌细胞结构和功能改变等众多调控环节,主要包括β肾上腺素和毒蕈碱受体系统、细胞膜物理特性和离子通道、高动力循环状态、体液因子(如一氧化氮、胆汁酸)等,但具体机制还需进一步研究3-5

    内皮细胞特异性分子1(endothelial cell specific-1,endocan)是一种可溶性、内皮衍生的硫酸皮肤素蛋白多糖,与炎症和血管生成有关。它具有活化血管内皮、抑制炎性细胞迁移的功能6。研究已经充分证明endocan参与了各种病理状态下的急性炎症和新血管形成机制,如败血症和肿瘤进展。近期研究7表明endocan可作为心血管疾病的诊断指标,与血管内皮功能障碍密切相关。另有研究8发现endocan是肝硬化患者的独立生存预测因子,肝硬化患者血清高endocan水平和高Child-Pugh分级预示低生存率,但是否参与CCM发病机制或者作为诊断标志物尚不明确,本研究通过对比肝硬化合并CCM患者和无CCM患者的血清endocan的水平及与肝硬化严重程度的关系,推测endocan在CCM发病机制中的可能作用。

    本研究为横断面研究,共连续入组2019年1月—2021年1月首都医科大学附属北京佑安医院住院的肝硬化患者。入组标准:年龄18~65岁,依据临床、实验室、超声和组织学检查结果诊断肝硬化。排除标准:合并急性发热或急性炎症反应综合征、重度贫血(血红蛋白<60 g/L)、酒精性肝病、原发性心血管疾病(如高血压、冠心病、风心病、缩窄性心包炎、心脏瓣膜病等)、甲状腺疾病、肾功能衰竭、急慢性呼吸系统疾病、糖尿病、恶性肿瘤等,近1周内服用对心脏功能有影响的药物(β受体阻滞剂、钙离子通道阻滞剂、血管紧张素转换酶抑制剂等)。根据有无CCM分为CCM组和无CCM组。CCM诊断标准符合2005年蒙特利尔世界胃肠病学大会制定的标准:收缩功能障碍(左心室射血分数<55%)和/或舒张功能障碍[3个标准中的至少2个:二尖瓣舒张早期血流早峰值E波和舒张晚期血流峰值A波(E/A)比值<1,E峰减容时间>200 ms,左心室等容舒张期时间延长>80 ms]。满足上述标准前提下还参考以下指标:心电图Q-T间期延长(QTc>0.440 s),脑尿钠肽(brain natriuretic peptide,BNP)、N端脑钠肽前体(N-terminal pro-brain natriuretic peptide,NT-proBNP)升高,心肌肌钙蛋白I(cTNI)升高。

    患者入院后立即收集患者的临床资料及实验室检查资料,包括年龄、性别、肝硬化病因、症状体征、合并疾病、血常规、肝肾功能、凝血项、心肌酶谱等,并计算出患者的Child-Pugh评分、终末期肝病模型(MELD)评分和MELD-Na评分用于评估肝硬化的严重程度。

    所有患者进行12导联心电图和超声心动图检查。超声心动图由经验丰富的首都医科大学附属北京佑安医院超声科专家专人操作,在iE33超声检查仪(飞利浦医疗系统,贝斯特,荷兰)上进行,并根据现行指南测量结构和功能参数。Fridericia公式(QTc=QT/RR0.33)用于计算矫正的QT间期。详细记录入组患者利尿剂的使用情况以避免药物对临床和超声参数的影响。

    所有入组患者和健康志愿者采集血清样本并在-80 °C下冷藏。采用间接法酶联免疫吸附试验(ELISA)法测定血清endocan,试剂盒购自法国Lunginnov公司,操作严格遵守说明书进行。将血清以3 000 r/min离心15 min,收集并分装储存在-80 ℃,使用前使试剂达到室温。所有样品一式两份进行测试。按照标准品的次序分别加入100 μL标准品、样品于空白微孔中,然后加入50 μL酶标记液,将孔密封并37 ℃避光孵育1 h。充分洗板5遍后每孔加入底物A、B各50 μL,将孔再次密封室温避光孵育10 min,最后各孔加入50 μL终止液,15 min内在450 nm波长处测定各孔的吸光度(OD)值。以所测标准品的OD值为横坐标,标准品的浓度值为纵坐标,在坐标纸上或用相关软件绘制标准曲线,并得到直线回归方程,将样品的OD值代入方程,计算出样品的浓度。

    采用Epidata 3.0进行数据录入,使用SPSS 26.0统计软件处理数据。正态分布的计量资料采用x¯±s表示,两组间比较采用成组t检验;偏态分布的计量资料采用MP25P75)表示,两组间比较采用Mann-Whitney U秩和检验。计数资料组间比较采用χ2检验。采用Pearson或Spearman相关分析进行相关性检验,应用受试者工作特征曲线(ROC曲线)评价CCM预测模型。P<0.05为差异有统计学意义。

    本研究共纳入肝硬化患者125例,其中无CCM组106例,CCM组19例,2组患者性别、年龄、肝硬化病因、实验室检查结果、肝硬化并发症、肝硬化严重程度(Child-Pugh分级、MELD评分及MELD-Na评分)比较,差异均无统计学意义(P值均>0.05),而NT-proBNP在CCM组表达量高于无CCM组,差异有统计学意义(P<0.05)(表1)。

    表  1  肝硬化CCM组及无CCM组患者一般资料比较
    Table  1.  Comparison of general data between CCM and no-CCM
    项目 CCM组(n=19) 无CCM组(n=106) 统计值 P
    男性[例(%)] 12(63.2) 71(67.0) χ2=2.834 0.632
    年龄(岁) 58.0±9.1 56.2±8.8 t=0.536 0.335
    肝硬化病因[例(%)] χ2=2.534 0.894
    HBV 5(26.3) 36(34.0)
    HCV 9(47.4) 42(39.6)
    原发性胆汁性胆管炎 1(5.3) 6(5.7)
    药物性肝损伤 4(21.1) 22(20.8)
    平均动脉压(mmHg) 89.7±11.0 87.0±9.8 t=0.043 0.291
    心率(次/min) 76.3±13.9 76.3±13.8 t=0.125 0.993
    Child-Pugh分级[例(%)] χ2=-2.134 0.172
    A级 12(63.2) 50(47.2)
    B级 4(21.1) 39(36.8)
    C级 3(15.8) 17(16.0)
    MELD评分(分) 6(5~7) 6(5~10) Z=-3.345 0.593
    MELD-Na评分(分) 8.1(5.1~10.2) 7.5(4.7~11.2) Z=-1.236 0.744
    ALT(U/L) 39.1(29.5~57.1) 25.8(15.4~38.5) Z=-0.232 0.552
    AST(U/L) 29.0(25.8~84.0) 39.1(29.2~57.1) Z=-0.134 0.361
    白蛋白(g/L) 31.4±0.5 31.8±0.2 t=0.123 0.762
    总胆红素(μmol/L) 25.9(18.4~33.7) 31.9(17.9~50.0) Z=-1.207 0.335
    肌酐(μmol/L) 59.3±0.5 62.1±0.23 t=0.042 0.553
    尿素氮(mmol/L) 4.4(3.8~5.7) 5.2(4.1~6.3) Z=-1.356 0.191
    国际标准化比值 1.2(1.1~1.5) 13.(1.2~1.5) Z=-2.237 0.493
    腹水[例(%)] 8(42.1) 64(60.4) χ2=0.018 0.227
    自发性腹膜炎[例(%)] 3(15.8) 13(12.3) χ2=0.346 0.961
    肝性脑病[例(%)] 1(5.3) 14(13.2) χ2=1.235 0.554
    食管静脉曲张[例(%)] 10(52.6) 70(66.0) χ2=0.234 0.397
    胃静脉曲张[例(%)] 6(31.6) 44(41.5) χ2=0.156 0.571
    门静脉内径(mm) 13(11~15) 13(12~14) Z=-1.239 0.857
    脾静脉内径(mm) 8(7~12) 10(8~12) Z=-1.670 0.144
    脾脏厚度(mm) 45.0±10.3 54.0±14.2 t=0.126 0.051
    白细胞(×109/L) 3.52(1.94~4.97) 3.99(2.24~5.23) Z=-0.467 0.633
    血红蛋白(g/L) 106.2±32.2 98.0±33.4 t=0.114 0.621
    血小板(×109/L) 74(48~129) 64(39~99) Z=-0.674 0.820
    血钠(mmol/L) 138.0±3.6 138.0±3.7 t=0.047 0.814
    血钾(mmol/L) 3.9(3.3~4.1) 3.8(3.5~4.1) Z=-1.345 0.886
    总胆固醇(mmol/L) 2.9±1.2 3.1±0.9 t=0.124 0.651
    甘油三酯(mmol/L) 0.8(0.6~1.1) 0.8(0.6~1.0) Z=-0.736 0.392
    NT-proBNP(pg/mL) 220(160~250) 119(108~160) Z=-3.028 <0.001
    cTNI(ng/mL) 0.27(0.21~0.28) 0.27(0.27~0.28) Z=-1.239 0.937
    使用利尿剂[例(%)] 8(42.1) 59(55.7) χ2=0.876 0.404
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    CCM组患者心脏收缩功能指标左心室射血分数、左室短轴缩短率及反映舒张功能指标E/A比值均显著低于无CCM组(P值均<0.05),而心电图指标QT间期在两组间比较,差异无统计学意义(表2)。

    表  2  肝硬化CCM组及无CCM组患者超声心动图和心电图各指标比较
    Table  2.  Comparison of echocardiography and electrocardiogram parameters between CCM and no-CCM
    参数 CCM组(n=19) 无CCM组(n=106) 统计值 P
    QT间期(ms) 397.1±31.1 398.2±31.7 t=0.053 0.832
    E/A比值 0.76(0.63~0.88) 0.98(0.77~1.30) Z=-5.789 <0.001
    左心室射血分数(%) 54.2±7.8 68.3±6.6 t=1.146 0.011
    左心房内径(mm) 34.6±4.5 34.5±5.1 t=0.347 0.963
    左心室舒张末内径(mm) 48.3±6.7 47.9±5.4 t=0.089 0.744
    左心室收缩末内径(mm) 32.2±7.5 29.1±4.5 t=0.157 0.096
    左室短轴缩短率(%) 34.3±5.7 39.8±4.5 t=3.248 <0.001
    左心室后壁厚度(mm) 10.1±1.7 8.9±1.5 t=1.324 0.064
    室间隔厚度(mm) 11.2(9.2~11.4) 10.6(9.3~11.6) Z=-1.663 0.161
    下载: 导出CSV 
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    采用ELISA法检测CCM组患者血清endocan的表达量为(2.69±0.43)ng/mL,明显高于肝硬化无CCM组(2.23±0.52)ng/mL(t=2.247,P=0.034)。

    根据肝功能Child-Pugh分级将所有入组的肝硬化患者分为代偿期组(Child-Pugh A级)62例和失代偿期组(Child-Pugh B、C级)63例,结果发现血清endocan水平在代偿期肝硬化组为(2.41±0.37)ng/mL,显著低于失代偿期肝硬化组(2.72±0.49)ng/mL(t=3.214,P=0.02)。其中在肝硬化代偿期患者中,CCM亚组(13例)血清endocan表达量为(2.60±0.44)ng/mL,显著高于肝硬化无CCM组(50例)(1.79±0.38)ng/mL(t=2.836,P=0.03),而在失代偿肝硬化患者中CCM亚组(6例)血清endocan表达量(2.73±0.45)ng/mL,无CCM亚组(56例)(2.67±0.48)ng/mL,两组差异无统计学意义(t=0.571,P=0.75)。

    在19例CCM患者中,血清endocan水平与肝功能Child-Pugh评分(r=0.509,P=0.026)、MELD-Na评分(r=0.484,P=0.036)呈正相关,与MELD评分(r=0.407,P=0.083)无明显相关性。血清endocan水平与反映门静脉压指标门静脉内径(r=-0.118,P=0.635)、脾静脉内径(r=-0.050,P=0.842)无明显相关性。

    在19例CCM患者中,血清endocan水平与平均动脉压(r=-0.591,P=0.013)呈负相关,与反映心脏舒张功能指标E/A比值(r=-0.515,P=0.042)呈负相关,而与反映心脏收缩功能指标左心室射血分数(r=-0.081,P=0.192)、左室短轴缩短率(r=-0.236,P=0.094)及心电图QT间期(r=0.131,P=0.67)无明显相关性,与血清NT-proBNP(r=0.074,P=0.251)、cTNI(r=0.085,P=0.276)无明显相关性。

    图1可知,血清endocan预测CCM的ROC曲线下面积(AUC)为0.658(95%CI:0.522~0.781),当截断值为2.61 ng/mL时,敏感度为67.1%,特异度为73.7%。由此推测血清endocan可能参与CCM发病机制,但对于是否可辅助诊断CCM尚需进一步扩大样本量研究。

    图  1  血清endocan预测CCM的ROC曲线
    Figure  1.  Serum endocan predicted ROC curve of CCM

    本研究发现肝硬化CCM患者血清endocan水平高于无CCM患者,并且与CCM患者的肝硬化严重程度呈正相关,与平均动脉压、心脏舒张功能指标E/A比值呈负相关,提示血清endocan与CCM的发生具有一定相关性,可能参与了CCM的发病机制。

    Endocan是一种新型糖蛋白,研究9-11表明主要由活化的肾血管内皮细胞、肺组织血管内皮细胞以及肿瘤血管内皮细胞分泌,但是它不仅局限于血管内皮细胞,部分增殖活跃的组织及新生组织中同样有表达。但在健康人群血清中表达水平很低。Endocan通过与细胞间黏附因子发挥相互作用,可有效抑制白细胞与血管内皮的结合。早有研究12显示endocan是血管内皮功能障碍及微血管炎症反应的潜在生物标志物。另有研究13-14报道血清endocan与慢性心功能不全患者的心功能障碍存在相关性,endocan与年龄、心功能纽约分级、左心室射血分数、NT-proBNP共同影响慢性心功能不全患者心血管终点事件的发生,且endocan对心血管事件的发生具有重要预测价值。尽管endocan具体作用机制尚未明确,但已经被越来越多地认为其与心血管系统疾病发病有关。

    目前endocan生成调节机制尚未不明确,但有研究结果已经显示,此过程可能有众多信号通路和生物活性物质的参与,如血管内皮生长因子A、白细胞介素1、TNF-α以及转化生长因子β1,均可以增加endocan的表达,而磷酸酰肌醇-3激酶和γ-干扰素则导致endocan表达降低15-17,在此过程中,血管内皮生长因子与其受体结合引起受体二聚化和细胞内络氨酸基团的反式磷酸化,调控细胞内磷脂酰肌醇-3-激酶/蛋白激酶B信号通路和蛋白激酶C/核因子κB信号通路活化,后者诱导endocan mRNA的表达,前者则发挥相反的作用。体外试验研究18-19也进一步验证了这一调控机制。

    研究20表明endocan参与肝脏血流动力学及微循环的改变。肝硬化患者肝内肝星状细胞被激活并合成endocan,endocan可以通过强烈收缩肝微循环使肝细胞缺氧,同时,肝星状细胞也是endocan作用的主要靶细胞,endocan可刺激肝星状细胞收缩、活化、增殖分泌出大量的基质,使肝血窦直径缩小,进而增加肝内血流阻力,导致肝血窦的血流量减少甚至完全停止,从而发生缺血、缺氧性损伤-肝循环障碍-门静脉高压形成。与此同时,肝组织局部缺血、缺氧又继续刺激endocan的合成和释放,形成恶性循环21。此外,endocan还与肝硬化患者发生细菌感染、疾病严重程度有关,并且是肝硬化预后不良的指标。也有研究22认为endocan是预测肝癌发生的生物标志物之一。

    本研究发现CCM组血清endocan显著高于无CCM组,而两组的肝功能无显著差异,提示该差异主要来源于CCM的存在。既往研究23表明炎症反应、肠道菌群异位引起的内毒素血症可以导致endocan升高,这表明在肝硬化心功能障碍的情况下endocan表达增加。在高血压人群,血清endocan水平与高血压的严重程度呈正相关24。本研究显示endocan在CCM组表达升高,在亚组分析中endocan与肝功能Child-Pugh评分和MELD-Na评分均相关,提示该指标仍然受到肝功能的影响,endocan与肝功能有关并且可能是肝硬化患者的独立生存预测因子。由于炎症和血管生成会增加血清endocan水平,而炎症和血管生成在肝硬化中都会逐渐严重改变,因此这些发现证实了笔者最初的假设。Voiosu等25目前的报道是唯一研究了endocan与肝硬化CCM关系的文章,结果显示肝硬化患者血清endocan显著高于健康人群,endocan预测CCM的AUC为0.64,该研究与本研究结果基本一致。

    总之,血清endocan在CCM患者中显著升高,并且与肝功能呈正相关,与平均动脉压呈负相关。提示endocan可能参与了CCM的发病机制,但是还不足以作为诊断指标。

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