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中华妇幼临床医学杂志(电子版)

中华妇幼临床医学杂志(电子版) ›› 2024, Vol. 20 ›› Issue (01) : 47 -57. doi: 10.3877/cma.j.issn.1673-5250.2024.01.007

论著

新辅助化疗联合间歇性肿瘤细胞减灭术对上皮性卵巢癌患者预后及血清学与影像学指标对患者预后的预测价值
何欣林1, 阎昊铮1, 赵亦非1, 江彩霞1, 李征宇1,†()   
  1. 1. 四川大学华西第二医院妇产科、出生缺陷与相关妇儿疾病教育部重点实验室，成都　610041
  • 收稿日期:2023-12-15 修回日期:2024-01-16 出版日期:2024-02-01
  • 通信作者: 李征宇

Prognosis of neoadjuvant chemotherapy combined with interval cytoreductive surgery and predictive value of serological and imaging indicators for optimal cytoreductive surgery in patients with epithelial ovarian cancer

Xinlin He1, Haozheng Yan1, Yifei Zhao1, Caixia Jiang1, Zhengyu Li1,†()   

  1. 1. Department of Obstetrics and Gynecology, Key Laboratory of Birth Defects and Related Disease of Women and Children, Ministry of Education, Reproductive Endocrinology and Regulation Laboratory, West China Second University Hospital, Sichuan University, Chengdu 610041, Sichuan Province, China
  • Received:2023-12-15 Revised:2024-01-16 Published:2024-02-01
  • Corresponding author: Zhengyu Li
  • Supported by:
    Natural Science Foundation of Sichuan Province(2023NSFSC0743)
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引用本文：

何欣林, 阎昊铮, 赵亦非, 江彩霞, 李征宇. 新辅助化疗联合间歇性肿瘤细胞减灭术对上皮性卵巢癌患者预后及血清学与影像学指标对患者预后的预测价值[J/OL]. 中华妇幼临床医学杂志(电子版), 2024, 20(01): 47-57.

Xinlin He, Haozheng Yan, Yifei Zhao, Caixia Jiang, Zhengyu Li. Prognosis of neoadjuvant chemotherapy combined with interval cytoreductive surgery and predictive value of serological and imaging indicators for optimal cytoreductive surgery in patients with epithelial ovarian cancer[J/OL]. Chinese Journal of Obstetrics & Gynecology and Pediatrics(Electronic Edition), 2024, 20(01): 47-57.

目的

探讨上皮性卵巢癌(EOC)患者接受新辅助化疗(NACT)联合间歇性肿瘤细胞减灭术(CS)治疗后的预后情况，并对EOC患者血清学与影像学指标对初次肿瘤细胞减灭术(PCS)后肉眼可见病灶完全切除，无残留病灶(R0)的预测价值。

方法

选择2014年3月至2018年7月于四川大学华西第二医院接受NACT联合间歇性CS治疗的129例EOC患者为研究对象。根据PCS是否达R0，将其分别纳入R0组(n＝72)与非R0组(n＝57)。入院后，收集2组患者PCS前、后血清糖类抗原125(CA125)水平、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)、血小板与淋巴细胞比值(PLR)等血清学指标，以及超声或CT检查的肿块最大径等影像学指标，分别采用CA125-1、NLR-1、LMR-1、PLR-1、肿块最大径-1，以及CA125-2、NLR-2、LMR-2、PLR-2、肿块最大径-2表示，对PCS前、后检查结果变化值，则采用CA125-ratio、NLR-ratio、LMR-ratio、PLR-ratio、肿块最大径-ratio表示，并采用Mann-Whitney U检验进行比较。绘制血清学与影像学指标预测EOC患者PCS达R0的受试者工作特征(ROC)曲线，并确定其预测的最佳临界值，计算各指标单一与联合预测EOC患者PCS达R0的预测效能。采用Cox比例风险回归分析，对R0组与非R0组、不同周期NACT满足血清学与影像学指标联合诊断标准EOC患者的总体生存(OS)与无进展生存(PFS)率进行比较。本研究遵循的程序符合2013年修订的《世界医学协会赫尔辛基宣言》要求。

结果

①R0组患者的OS率(60.0%)较非R0组(28.6%)高，并且差异有统计学意义(HR＝0.370，95%CI：0.194～0.703，P＝0.002)。R0组PFS率(40.3%)与非R0组(54.4%)比较，差异无统计学意义(P＝0.122)。②R0组与非R0组EOC患者CA125-ratio、NLR-2和LMR-2分别比较，差异均有统计学意义(Z＝－3.09、－2.14、－2.40，P＝0.002、0.033、0.017)，2组PLR-Ratio比较，差异无统计学意义(P＝0.912)。③绘制CA125-ratio、1－NLR-2、LMR-2及肿块最大径-ratio预测EOC患者PCS后是否达R0的ROC曲线结果显示，根据约登指数最大原则，预测EOC患者PCS后达R0的最佳临界值为CA125-ratio>93.64%，NLR-2<2.14，LMR-2>4.34，此时其阳性预测值分别为71.0%、65.6%、68.2%；根据实体瘤疗效评价标准(RECIST) 1.1，采用肿块最大径-ratio>20%预测EOC患者PCS后达R0的阳性预测值为62.9%。当患者满足CA125-ratio>93.6%、NLR-2<2.14、LMR-2>4.34、肿块最大径-ratio>20%这4项指标中≥3项或4项时，其预测EOC患者PCS后达R0的阳性预测值分别为75.7%与88.2%。④Cox比例风险回归分析结果显示，对不同周期NACT(<3个、3个与>3个周期)满足上述≥3项指标EOC患者的OS曲线比较，差异无统计学意义(P>0.05)，但是随着NACT周期增加，EOC患者OS率呈下降趋势。

结论

采取NACT联合间歇性CS治疗EOC患者，PCS后达R0者OS率高于未达R0者。将CA125-ratio>93.6%、NLR-2<2.14、LMR-2>4.34、肿块最大径-ratio>20%联合预测EOC患者NACT后进行PCS达R0的阳性预测值，较单一指标预测的阳性预测值更高。当EOC患者满足上述指标≥3项时，及时终止NACT可能有助于患者获得更高OS率。

关键词: 卵巢肿瘤, 新辅助化疗, 肿瘤细胞减灭术, CA-125抗原, 中性粒细胞与淋巴细胞比值, 淋巴细胞与单核细胞比值, 血小板与淋巴细胞比值, 妇女
Objective

To investigate the prognosis of neoadjuvant chemotherapy (NACT) combined with interval cytoreductive surgery (CS) in treatment of patients with epithelial ovarian cancer (EOC), and analyze the predictive value of serological and imaging indicators in EOC patients for reaching macroscopic residual lesion naught (R0) after primary cytoreductive surgery (PCS).

Methods

A total of 129 EOC patients who underwent NACT combined with interval CS in West China Second University Hospital, Sichuan University from March 2014 to July 2018 were enrolled as research subjects. Patients were enrolled into R0 group (n=72) and non-R0 group (n=57) according to whether the patients reached R0 after PCS. The serological indicators of two groups were collected, including the serum level of carbohydrate antigen 125 (CA125), neutrophil-to-lymphocyte ratio (NLR), lymphocyte-monocyte ratio (LMR), platelet-to-lymphocyte ratio (PLR) and the image indicator (maximum diameter of tumor on ultrasound or CT examination) of patients before and after PCS. Results of examinations before PCS was recorded as CA125-1, NLR-1, LMR-1, PLR-1 and maximum diameter-1, and results of examinations after PCS was recorded as CA125-2, NLR-2, LMR-2, PLR-2 and maximum diameter-2. The change values between them were recorded as CA125-ratio, NLR-ratio, LMR-ratio, PLR-ratio, and maximum diameter-ratio. Mann-Whitney U test was used for comparison of these indicators between the R0 and non-R0 groups. The receiver operating characteristic (ROC) curve of serological and imaging indicators in predicting R0 in PCS of EOC patients was plotted, and the optimal cut-off value for prediction was determined. The prediction performance of single and combined indicators in predicting R0 in PCS of EOC patients was calculated. Cox proportional hazards regression analysis was used to compare the overall survival (OS) and progression-free survival (PFS) curves of EOC patients in the R0 and non-R0 groups and patients under different NACT cycles that met the combined diagnostic criteria of serological and imaging indicators. The procedures followed in this study were in line with the requirements of the World Medical Association Declaration of Helsinki revised in 2013.

Results

①The OS rate of R0 group (60.0%) was higher than that of non-R0 group (28.6%), and the difference was statistically different (HR=0.370, 95%CI: 0.194-0.703, P=0.002). There was no significant difference in PFS rate between R0 group (40.3%) and non-R0 group (54.4%) (P=0.122). ②The differences in CA125-ratio, NLR-2 and LMR-2 between R0 group and non-R0 group were statistically significant (Z=-3.09, -2.14, -2.40; P=0.002, 0.033, 0.017), but there was no significant difference in PLR-ratio between two groups (P=0.912). ③Results of the ROC curve of CA125-ratio, 1-NLR-2, LMR-2 and maximum diameter-ratio for predicting R0 in PCS of EOC patients showed that the optimal cutoff value for prediction of achieve R0 was CA125-ratio>93.64%, NLR-2<2.14, LMR-2>4.34 according to the principle of maximum Youden index, and their positive predictive values were 71.0%, 65.6%, and 68.2 %, respectively. According to response evaluation criteria in solid tumors (RECIST) 1.1, maximum diameter-ratio >20% was used to predict R0 in PCS of EOC patients, and its positive predictive value was 62.9%. Combining these four indicators, when the patient met ≥3 or 4 of CA125-ratio>93.6%, NLR-2<2.14, LMR-2>4.34, and maximum diameter-ratio>20%, its positive predictive values of achieving R0 in EOC patients were 75.7% and 88.2%, respectively. ④Results of Cox proportional hazards regression analysis showed that there was no significant difference in the OS curves of EOC patients with different NACT cycles (< 3, 3 and >3 cycles) that met ≥3 of the above indicators (P>0.05), but with the increase of NACT cycles, the OS rate of EOC patients showed a downward trend.

Conclusions

The OS rate of EOC patients who reach R0 in PCS after NACT is higher than that of those who do not reach R0. The positive predictive value of combination of CA125-ratio >93.6%, NLR-2<2.14, LMR-2>4.34 and maximum diameter-ratio>20% for prediction of R0 in EOC patients is higher than the positive predictive value predicted by a single indicator. When patients with EOC meet ≥3 of the above indicators, the termination of NACT may help patients achieve higher OS rates.

Key words: Ovarian neoplasms, Neoadjuvant chemotherapy, Cytoreduction surgical procedures, CA-125 antigen, Neutrophil-to-lymphocyte ratio, Lymphocyte-to-monocyte ratio, Platelet-to-lymphocyte ratio, Women
表1 129例ECO患者一般临床资料分析[例数(%)]
临床项目 发生率 临床项目 发生率
是否绝经 ASA分级(级)
是 73(56.6) 1 2(1.6)
否 56(43.4) 2 99(76.7)
内科合并症 3 28(21.7)
高血压 19(14.7) NACT方案  
贫血 6(4.7) TP 123(95.3)
心脏衰竭 1(0.8) CP 2(1.6)
慢性阻塞性肺疾病 1(0.8) TP＋CP 4(3.1)
糖尿病 6(4.7) FIGO分期(期)  
肝炎 9(7.0) Ⅲ 116(89.9)
胃炎 2(1.6) Ⅳ 13(10.1)
尿路结石 3(2.3) 是否达R0  
静脉血栓 2(1.6) 是 72(55.8)
其他 2(1.6) 否 57(44.2)
无内科合并症 78(60.5) 术后化疗周期数(个)  
NACT周期数(个) ≤6 41(31.8)
1～2 44(34.1) 7～12 77(59.7)
3 62(48.1) >12 11(8.5)
4 18(13.9)    
≥5 5(3.9)    
图1 采用Cox比例风险回归分析方法绘制的EOC患者OS及PFS曲线(图1A：所有患者OS曲线；图1B：R0组与非R0组OS曲线；图1C：所有患者PFS曲线；图1D：R0组与非R0组PFS曲线)注：EOC为上皮性卵巢癌，OS为总体生存，PFS无进展生存。R0组指初次肿瘤细胞减灭术中无肉眼可见残留病灶，非R0组指初次肿瘤细胞减灭术中有肉眼可见残留病灶
表2 EOC患者OS期影响因素的多因素Cox比例风险回归分析结果
临床因素 B SE Wald值 P值 HR值 HR值95%CI
年龄 －0.018 0.033 0.307 0.580 0.982 0.920～1.047
未绝经 －0.167 0.497 0.113 0.737 0.846 0.319～2.242
BMI －0.068 0.054 1.558 0.212 0.934 0.840～1.039
ASA分级(vs ASA分级为1级)            
2级 0.601 1.970 0.093 0.760 1.824 0.038～86.660
3级 0.446 0.439 1.030 0.310 1.562 0.660～3.694
术前合并症 －0.241 0.361 0.447 0.504 0.786 0.387～1.594
NACT周期数(vs 1个NACT周期)            
2个 0.607 2.390 0.065 0.799 1.835 0.017～198.440
3个 1.447 2.339 0.382 0.536 4.249 0.043～416.479
4个 1.384 2.313 0.358 0.550 3.991 0.043～371.488
5个 －11.020 510.599 <0.001 0.983 <0.001 <0.001
6个 2.767 2.553 1.175 0.278 15.912 0.107～2 368.330
化疗方案(vs TP)            
CP 1.253 1.080 1.346 0.246 3.503 0.421～29.106
TP＋CP －10.796 510.504 <0.001 0.983 <0.001 <0.001
盆腔淋巴结切除 －0.405 0.492 0.679 0.410 0.667 0.254～1.748
腹主动脉旁淋巴结切除 0.487 0.447 1.186 0.276 1.627 0.678～3.907
合并腹水 0.450 0.353 1.623 0.203 1.568 0.785～3.131
手术时间 －0.001 0.002 0.346 0.557 0.999 0.995～1.003
术中输血 －0.396 0.388 1.042 0.307 0.673 0.315～1.440
FIGO分期为Ⅳ期(vsⅢ期) －0.891 0.583 2.335 0.126 0.410 0.131～1.286
达R0 －0.996 0.328 9.208 0.002 0.370 0.194～0.703
未使用白蛋白 0.152 0.480 0.100 0.752 1.164 0.454～2.985
术后输血 0.183 0.454 0.162 0.687 1.201 0.493～2.923
总住院天数 0.201 0.064 9.963 0.002 1.223 1.079～1.385
ICU住院天数 －0.288 0.251 1.323 0.250 0.750 0.459～1.225
术后至化疗间隔时间 0.051 0.020 6.418 0.011 1.052 1.012～1.095
术后化疗次数 －0.038 0.040 0.902 0.342 0.963 0.891～1.041
表3 EOC患者PFS期影响因素的多因素Cox比例风险回归分析结果
临床因素 B SE Wald值 P值 HR值 HR值95%CI
年龄 0.003 0.037 0.013 0.909 1.003 0.932～1.079
未绝经 0.653 0.621 1.108 0.293 1.922 0.569～6.489
BMI －0.087 0.055 2.538 0.111 0.916 0.823～1.020
ASA分级(vs ASA分级为1级)            
2级 0.705 1.493 0.223 0.637 2.024 0.109～37.715
3级 －1.037 0.446 5.404 0.020 0.354 0.148～0.850
术前合并症 0.826 0.583 2.008 0.157 2.284 0.729～7.157
NACT周期数(vs 1个NACT周期)            
2个 2.137 1.756 1.482 0.224 8.474 0.271～264.496
3个 －0.146 1.317 0.012 0.912 0.864 0.065～11.415
4个 0.359 1.309 0.075 0.784 1.432 0.110～18.643
5个 0.527 1.238 0.181 0.671 1.693 0.150～19.170
6个 －1.316 1.464 0.808 0.369 0.268 0.015～4.728
化疗方案(vs TP)            
CP －0.732 0.895 0.667 0.414 0.481 0.083～2.786
TP＋CP 1.169 1.515 0.596 0.440 3.219 0.165～62.673
盆腔淋巴结切除 －0.070 0.816 0.007 0.932 0.933 0.188～4.165
腹主动脉旁淋巴结切除 1.120 0.614 3.329 0.068 3.065 0.920～10.212
合并腹水 0.827 0.384 4.645 0.031 2.288 1.078～4.855
手术时间 0.004 0.003 1.725 0.189 1.004 0.998～1.011
术中输血 0.613 0.545 1.262 0.261 1.845 0.634～5.374
FIGO分期为Ⅳ期(vsⅢ期) －0.498 0.699 0.508 0.261 1.845 0.634～5.374
达R0 0.585 0.378 2.395 0.122 1.794 0.856～3.762
未使用白蛋白 0.100 0.487 0.043 0.837 1.106 0.425～2.875
术后输血 0.982 0.483 4.138 0.042 2.669 1.036～6.873
总住院天数 －0.187 0.113 2.725 0.099 0.830 0.665～1.036
ICU住院天数 －0.346 0.282 1.510 0.219 0.707 0.407～1.229
术后至化疗间隔时间 0.089 0.026 11.829 0.001 1.094 1.039～1.151
术后化疗次数 －0.090 0.073 1.516 0.218 0.914 0.791～1.055
表4 R0组与非R0组EOC患者血清学指标比较[M(Q1，Q3)]
组别 例数 CA125-ratio(%) PLR-ratio(%) NLR-2 LMR-2
R0组 72 96.4(90.9，98.1) 55.8(34.8，68.0) 5.1(97.1，167.8) 123.7(4.6，7.1)
非R0组 57 92.0(77.5，96.9) 49.5(41.3，68.4) 2.4(1.7，3.2) 4.3(3.6，6.3)
Z值   －3.09 －0.11 －2.14 －2.40
P值   0.002 0.912 0.033 0.017
图2 血清学指标与肿块最大径-ratio预测EOC患者PCS达R0的ROC曲线注：CA125-ratio、肿块最大径-ratio计算公式为(1－PCS前最后1次检查结果/入院后第1次检查结果)×100%。NLR-2、LMR-2指PCS前最后1次检查的NLR、LMR。R0指PCS中无肉眼可见残留病灶。EOC为上皮性卵巢癌，PCS为初次肿瘤细胞减灭术，ROC曲线为受试者工作特征曲线。CA125为糖类抗原125，PLR为血小板与淋巴细胞比值，NLR为中性粒细胞与淋巴细胞比值，LMR为淋巴细胞与单核细胞比值
表5 血清学指标与肿块最大径-ratio单独及联合预测EOC患者PCS达R0的预测效能
预测指标 最佳临界值 敏感度(%) 特异度(%) 阳性预测值(%) 约登指数
CA125-ratio 93.6% 68.1 64.9 71.0 0.33
NLR-2 2.14 55.6 63.2 65.6 0.19
LMR-2 4.34 80.6 52.6 68.2 0.33
肿块最大径-ratio 20% 78.0 42.5 62.9 0.21
满足任意1项指标 — 97.2 19.3 60.3 0.16
满足任意2项指标 — 81.9 50.9 67.8 0.33
满足任意3项指标 — 55.6 77.2 75.7 0.33
满足4项指标 — 20.8 96.5 88.2 0.17
图3 不同NACT周期数满足CA125-ratio>93.6%、NLR-2<2.14、LMR-2>4.34、肿块最大径-ratio>20%这4项指标或满足其中≥3项指标的EOC患者的OS曲线(图3A：满足4项指标的EOC患者；图3B：满足≥3项指标的EOC患者)注：CA125-ratio、肿块最大径-ratio计算公式为(1－PCS前最后1次检查结果/入院后第1次检查结果)×100%。NLR-2、LMR-2指PCS前最后1次检查的NLR、LMR。R0指PCS中无肉眼可见残留病灶。NACT为新辅助化疗，EOC为上皮性卵巢癌，OS为总体生存。CA125为糖类抗原125，PLR为血小板与淋巴细胞比值，NLR为中性粒细胞与淋巴细胞比值，LMR为淋巴细胞与单核细胞比值，PCS为初次肿瘤细胞减灭术
表6 不同NACT周期数EOC患者OS期的Cox比例风险回归分析结果
临床因素 B SE Wald值 P值 HR值 HR值95%CI
不同NACT周期数(vs NACT周期数<3个)a            
NACT周期数为3个 －0.804 0.732 1.208 0.272 0.448 0.107～1.877
NACT周期数>3个 －0.587 0.587 1.002 0.317 0.556 0.176～1.755
不同NACT周期数(vs NACT周期数≤3个)b －0.070 1.157 0.004 1.000 0.952 0.932～8.994
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