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胃癌是最常见的恶性肿瘤之一。2020年全球癌症统计数据显示,在185个国家或地区的36种癌症中,胃癌的发病率居第5位,病死率居第4位[1]。我国胃癌患者总体5年生存率不足50%[2],转移和术后复发是其预后差的主要原因,其中淋巴结转移是主要危险因素之一[3]。评估淋巴结转移的重要指标之一是淋巴结大小,但胃癌患者中超过60%的转移淋巴结小于8 mm[4],导致CT检出率较低。通过18F-FDG PET/CT显像中葡萄糖代谢情况和淋巴结短径综合评估淋巴结转移,从而提高术前淋巴结分期的准确性[5]。然而,在临床上综合评估为N0期的胃癌患者中,仍可发现11%~56%的患者术后存在淋巴结转移[6-7],即隐匿性淋巴结转移(occult lymph node metastasis,OLM)。存在OLM的患者更易出现肿瘤复发,预后较差[8]。因此, OLM的早期确诊对临床医师精准制定治疗方案及预后评估具有重要意义。18F-FDG PET/CT有多个异质性指数(heterogeneity index, HI),如变异系数[9]、线性回归斜率[10]等,有研究者发现HI对于多种恶性肿瘤的OLM具有预测价值[11-12]。目前采用HI预测胃癌患者的OLM尚无有效依据。胃腺癌是胃癌最常见的类型,本研究旨在探讨胃腺癌患者术前18F-FDG PET/CT显像中原发灶的肿瘤内代谢HI对胃癌OLM的预测价值。
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由表1可知,OLM阳性组与OLM阴性组间性别、分化程度及病理T分期差异均有统计学意义(均P<0.05),年龄、肿瘤原发灶部位、分化程度、Lauren分型、CA199水平升高和CEA水平升高组间差异均无统计学意义(均P>0.05)。
组别 年龄
(岁, ±s)$ \stackrel{-}{x} $ 性别(例,%) 肿瘤原发灶部位(例,%) 分化程度(例,%) 男 女 GEJ及
胃底部胃体及
大小弯胃窦及
幽门区中分化 中-低分化 低分化 OLM阳性组(n=39) 62.82±10.48 27(69.2) 12(30.8) 16(41.0) 11(28.2) 12(30.8) 8(20.5) 12(30.8) 19(48.7) OLM阴性组(n=40) 64.80±7.22 35(87.5) 5(12.5) 21(52.5) 9(22.5) 10(25.0) 17(42.5) 13(32.5) 10(25.0) 检验值 z=−0.196 x2=3.903 x2=1.045 x2=6.061 P值 0.844 0.048 0.593 0.048 组别 Lauren分型(例,%) 病理T分期(例,%) CA199水平升高(例,%) CEA水平升高(例,%) 肠型 弥漫型 混合型 T1~T2 T3~T4 OLM阳性组(n=39) 16(41.0) 11(28.2) 12(30.8) 5(12.8) 34(87.2) 5(13.5) 4(10.8) OLM阴性组(n=40) 24(60.0) 9(22.5) 7(17.5) 15(37.5) 25(62.5) 7(18.9) 4(10.8) 检验值 x2=3.104 x2=6.361 x2=0.398 0 P值 0.212 0.012 0.528 1.00 表 1 胃腺癌隐匿性淋巴结转移阳性组与阴性组患者的临床特征比较
Table 1. Comparison of clinical characteristics between the positive and negative groups in patients with occult lymph node metastasis of gastric adenocarcinoma
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由表2可知, OLM阳性组原发灶HI-2明显高于OLM阴性组,且差异有统计学意义(P<0.05);而OLM阴性组原发灶SUVmax、SUVmean 、HI-1均明显高于OLM阳性组,且差异均有统计学意义(均P<0.05)。
组别 SUVmax SUVpeak SUVmean TLR MTV(cm3) TLG(g) HI-1 HI-2 OLM阳性组(n=39) 5.59
(4.46,7.51)4.37
(3.23,5.38)3.33
(3.06,3.85)2.75
(2.20,3.70)11.94
(3.23,30.90)39.87
(9.48,113.88)0.23±0.12 4.98
(2.68,8.44)OLM阴性组(n=40) 6.91
(5.11,10.64)5.09
(3.90,7.21)3.65
(3.25,4.64)3.30
(2.42,5.36)12.32
(3.37,20.86)43.07
(11.69,90.10)0.29±0.14 2.61
(1.84,4.23)检验值 z=−2.000 z=−1.736 z=−2.001 z=−1.314 z=−0.074 z=−0.255 t=2.096 z=−3.178 P值 0.045 0.083 0.045 0.189 0.941 0.799 0.039 0.001 表 2 胃腺癌隐匿性淋巴结转移阳性组与阴性组患者18F-FDG PET/CT代谢参数的比较[M(Q1,Q3)或
±s]$ \bar{x} $ Table 2. Comparison of metabolic parameters of 18F-FDG PET/CT between positive and negative groups of patients with occult lymph node metastasis in patients with occult lymph node metastasis of gastric adenocarcinoma [M(Q1, Q3) or
±s]$ \bar{x} $ -
由表3单因素Logistic回归模型分析结果可知,分化程度、病理T分期、HI-1和HI-2是OLM的危险因素;由表3多因素Logistic回归模型分析结果可知,病理T分期和HI-2是胃腺癌患者OLM的独立危险因素。
临床特征和代谢参数 单因素分析
OR(95%CI)P值 多因素分析
OR(95%CI)P值 分化程度 0.054 0.174 中分化 1.000 1.000 中-低分化 1.962(0.621~6.193) 0.251 1.667(0.432~6.435) 0.459 低分化 4.037(1.295~12.585) 0.016 3.467(0.918~13.096) 0.067 病理T分期 T1-T2 1.000 1.000 T3-T4 4.080(1.310~12.709) 0.015 4.780(1.238~18.458) 0.023 SUVmax 0.891(0.792~1.003) 0.055 SUVpeak 0.877(0.758~1.014) 0.076 SUVmean 0.602(0.361~1.005) 0.052 TLR 0.808(0.631~1.034) 0.090 MTV(cm3) 0.999(0.977~1.021) 0.901 TLG(g) 0.998(0.994~1.003) 0.430 HI-1 0.025(0.001~0.992) 0.045 0.537(0.007~39.527) 0.777 HI-2 >4.962 7.368(2.385~22.764) <0.001 6.893(1.922~24.718) 0.003 ≤4.962 1.000 1.000 注:FDG为氟脱氧葡萄糖;PET为正电子发射断层显像术;CT为计算机体层摄影术;SUVmax为最大标准化摄取值;SUVpeak为标准化摄取值峰值;SUVmean为平均标准化摄取值;TLR为原发灶SUVmax/肝脏SUVmean的比值;MTV为肿瘤代谢体积;TLG为糖酵解总量;HI为异质性指数;CI为置信区间 表 3 胃腺癌隐匿性淋巴结转移患者临床特征和18F-FDG PET/CT代谢参数的单因素及多因素Logistic回归模型分析
Table 3. Logistic univariate and multivariate regression analysis of clinical characteristics and 18F-FDG PET/CT metabolic parameters in patients with occult lymph node metastasis of gastric adenocarcinoma
ROC曲线分析结果显示,HI-1预测OLM的AUC为0.360(95%CI:0.237~0.483,P=0.001),因此HI-1不具有诊断价值。HI-2预测OLM的AUC为0.708(95%CI:0.593~0.822,P<0.05)(图1),因此HI-2对OLM的诊断具有较好的准确率。当以最佳临界值4.962进行预测时,其诊断OLM的灵敏度和特异度分别为51.3%(20/39)和87.5%(35/40),典型患者图像见图2。
18F-FDG PET/CT肿瘤内代谢异质性指数预测胃腺癌隐匿性淋巴结转移的价值
Value of 18F-FDG PET/CT intra-tumor metabolic heterogeneity index for predicting occult lymph node metastasis in gastric adenocarcinoma
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摘要:
目的 评估术前18F-氟脱氧葡萄糖(FDG) PET/CT原发灶肿瘤内代谢异质性指数(HI)对胃腺癌隐匿性淋巴结转移(OLM)的预测价值。 方法 回顾性分析2016年1月至2022年12月于郑州大学第一附属医院术前行18F-FDG PET/CT检查的79例胃腺癌患者的临床资料,其中男性62例、女性17例,年龄(63.8±9.0)岁。所有患者均于18F-FDG PET/CT显像后1个月内行胃腺癌根治术,根据术后组织病理学检查结果分为OLM阳性组(n=39)和OLM阴性组(n=40)。采用卡方检验、两独立样本t检验(方差齐)和Mann-Whitney U检验对胃腺癌患者的临床特征、18F-FDG PET/CT代谢参数进行组间比较。采用单因素及多因素logistic回归模型分析预测OLM的独立危险因素。采用受试者工作特征(ROC)曲线分析HI对OLM的诊断效能。 结果 OLM阳性组与OLM阴性组间性别、分化程度及病理T分期差异均有统计学意义(x2=3.903~6.361,均P<0.05)。OLM阳性组原发灶HI-2明显高于OLM阴性组[4.98(2.68,8.44)对2.61(1.84,4.23)],且差异有统计学意义(z=−3.178,P<0.05);而OLM阴性组原发灶SUVmax、SUVmean、HI-1 [5.59(4.46,7.51)对6.91(5.11,10.64)=、3.33(3.06,3.85)对3.65(3.25,4.64)=、(0.23±0.12) 对(0.29±0.14)]均明显高于OLM阳性组,且差异均有统计学意义(z=−2.000、-2.001,t=2.096;均P<0.05)。单因素Logistic回归模型分析结果显示,分化程度(OR=4.037,95%CI:1.295~12.585,P<0.05)、病理T分期(OR=4.080,95%CI:1.310~12.709,P<0.05)、HI-1(OR=0.025,95%CI:0.001~0.992,P<0.05)和HI-2(OR=7.368,95%CI:2.385~22.764,P<0.001)是OLM的危险因素;多因素logistic回归模型分析结果显示,病理T分期(OR=4.780,95%CI:1.238~18.458,P<0.05)和HI-2(OR=6.893,95%CI:1.922~24.718,P<0.05)是胃腺癌患者OLM的独立危险因素。ROC曲线分析结果显示,HI-2预测OLM的ROC曲线下面积(AUC)为0.708(95%CI :0.237~0.483,P=0.001),当以其最佳临界值4.962进行预测时,其诊断OLM的灵敏度和特异度分别为51.3%(20/39)和87.5%(35/40)。 结论 胃腺癌术前18F-FDG PET/CT原发灶肿瘤内代谢HI对胃腺癌OLM具有预测价值,且HI-2是OLM的独立危险因素。 -
关键词:
- 胃肿瘤 /
- 淋巴结 /
- 肿瘤转移 /
- 正电子发射断层显像术 /
- 体层摄影术,X线计算机 /
- 脱氧葡萄糖
Abstract:Objective To investigate the predictive value of 18F-fluorodeoxyglucose(FDG) PET/CT primary lesions metabolic heterogeneity index for occult lymph node metastasis(OLM) in gastric cancer. Methods A retrospective analysis was performed on 79 patients [62 males, 17 females, age (63.8±9.0) years] with gastric cancer who underwent 18F-FDG PET/CT imaging and were diagnosed as clinical (c)N0 stage before surgery from January 2016 to December 2022 in the First Affiliated Hospital of Zhengzhou University. All patients underwent radical gastrectomy in our hospital within 1 month after imaging, and were divided into OLM-positive group and OLM-negative group according to postoperative pathology to determine whether there was lymph node metastasis. The following PET/CT parameters were measured: The maximum, mean and peak normalized uptake values (SUVmax, SUVmean, SUVpeak) , tumor metabolic volume (MTV) and total focal glycolysis (TLG)of the primary lesions.And TLR (tumor - liver ratio), heterogeneity index -1 (HI-1) and heterogeneity index -2 (HI-2) were calculated. The t test and Mann-Whitney U test of two independent samples were used to compare the parameters between groups. The independent risk factors of OLM were analyzed by logistic regression. The diagnostic efficacy of heterogeneity index on OLM was analyzed by receiver operating characteristic (ROC) curve. Results A total of 39 (49.4%, 39/79) of the 79 patients were pathologically confirmed to have OLM. HI-2 in OLM positive group was higher than that in OLM negative group [4.98 (2.68, 8.44) vs 2.61 (1.84, 4.23), z=−3.178, P < 0.05], while SUVmax in OLM negative group was higher than that in OLM negative group [5.59 (4.46, 7.51) vs 6.91 (5.11, 10.64). z=−2.000, P < 0.05], SUVmean[3.33 (3.06, 3.85) vs 3.65 (3.25, 4.64), z=−2.001, P < 0.05], HI-1[0.23±0.12 vs 0.29±0.14, t=2.096, P < 0.05] were significantly higher than those in OLM positive group. Multivariate logistic regression analysis showed that HI-2 was an independent risk factor for OLM [odds ratio (OR) =6.893, 95%CI: 1.922-24.718, P < 0.05]. The area under ROC curve (AUC) of HI-2 for OLM prediction was 0.708 (95%CI: 0.237-0.483, P=0.001), and the sensitivity and specificity for OLM diagnosis were 51.3% (20/39) and 87.5% (35/40), respectively, when the threshold was 4.962. Conclusion 18F-FDG PET/CT tumor metabolic heterogeneity index has predictive value for OLM in gastric cancer, and heterogeneity index -2 is an independent risk factor for OLM. -
表 1 胃腺癌隐匿性淋巴结转移阳性组与阴性组患者的临床特征比较
Table 1. Comparison of clinical characteristics between the positive and negative groups in patients with occult lymph node metastasis of gastric adenocarcinoma
组别 年龄
(岁, ±s)$ \stackrel{-}{x} $ 性别(例,%) 肿瘤原发灶部位(例,%) 分化程度(例,%) 男 女 GEJ及
胃底部胃体及
大小弯胃窦及
幽门区中分化 中-低分化 低分化 OLM阳性组(n=39) 62.82±10.48 27(69.2) 12(30.8) 16(41.0) 11(28.2) 12(30.8) 8(20.5) 12(30.8) 19(48.7) OLM阴性组(n=40) 64.80±7.22 35(87.5) 5(12.5) 21(52.5) 9(22.5) 10(25.0) 17(42.5) 13(32.5) 10(25.0) 检验值 z=−0.196 x2=3.903 x2=1.045 x2=6.061 P值 0.844 0.048 0.593 0.048 组别 Lauren分型(例,%) 病理T分期(例,%) CA199水平升高(例,%) CEA水平升高(例,%) 肠型 弥漫型 混合型 T1~T2 T3~T4 OLM阳性组(n=39) 16(41.0) 11(28.2) 12(30.8) 5(12.8) 34(87.2) 5(13.5) 4(10.8) OLM阴性组(n=40) 24(60.0) 9(22.5) 7(17.5) 15(37.5) 25(62.5) 7(18.9) 4(10.8) 检验值 x2=3.104 x2=6.361 x2=0.398 0 P值 0.212 0.012 0.528 1.00 表 2 胃腺癌隐匿性淋巴结转移阳性组与阴性组患者18F-FDG PET/CT代谢参数的比较[M(Q1,Q3)或
±s]$ \bar{x} $ Table 2. Comparison of metabolic parameters of 18F-FDG PET/CT between positive and negative groups of patients with occult lymph node metastasis in patients with occult lymph node metastasis of gastric adenocarcinoma [M(Q1, Q3) or
±s]$ \bar{x} $ 组别 SUVmax SUVpeak SUVmean TLR MTV(cm3) TLG(g) HI-1 HI-2 OLM阳性组(n=39) 5.59
(4.46,7.51)4.37
(3.23,5.38)3.33
(3.06,3.85)2.75
(2.20,3.70)11.94
(3.23,30.90)39.87
(9.48,113.88)0.23±0.12 4.98
(2.68,8.44)OLM阴性组(n=40) 6.91
(5.11,10.64)5.09
(3.90,7.21)3.65
(3.25,4.64)3.30
(2.42,5.36)12.32
(3.37,20.86)43.07
(11.69,90.10)0.29±0.14 2.61
(1.84,4.23)检验值 z=−2.000 z=−1.736 z=−2.001 z=−1.314 z=−0.074 z=−0.255 t=2.096 z=−3.178 P值 0.045 0.083 0.045 0.189 0.941 0.799 0.039 0.001 表 3 胃腺癌隐匿性淋巴结转移患者临床特征和18F-FDG PET/CT代谢参数的单因素及多因素Logistic回归模型分析
Table 3. Logistic univariate and multivariate regression analysis of clinical characteristics and 18F-FDG PET/CT metabolic parameters in patients with occult lymph node metastasis of gastric adenocarcinoma
临床特征和代谢参数 单因素分析
OR(95%CI)P值 多因素分析
OR(95%CI)P值 分化程度 0.054 0.174 中分化 1.000 1.000 中-低分化 1.962(0.621~6.193) 0.251 1.667(0.432~6.435) 0.459 低分化 4.037(1.295~12.585) 0.016 3.467(0.918~13.096) 0.067 病理T分期 T1-T2 1.000 1.000 T3-T4 4.080(1.310~12.709) 0.015 4.780(1.238~18.458) 0.023 SUVmax 0.891(0.792~1.003) 0.055 SUVpeak 0.877(0.758~1.014) 0.076 SUVmean 0.602(0.361~1.005) 0.052 TLR 0.808(0.631~1.034) 0.090 MTV(cm3) 0.999(0.977~1.021) 0.901 TLG(g) 0.998(0.994~1.003) 0.430 HI-1 0.025(0.001~0.992) 0.045 0.537(0.007~39.527) 0.777 HI-2 >4.962 7.368(2.385~22.764) <0.001 6.893(1.922~24.718) 0.003 ≤4.962 1.000 1.000 注:FDG为氟脱氧葡萄糖;PET为正电子发射断层显像术;CT为计算机体层摄影术;SUVmax为最大标准化摄取值;SUVpeak为标准化摄取值峰值;SUVmean为平均标准化摄取值;TLR为原发灶SUVmax/肝脏SUVmean的比值;MTV为肿瘤代谢体积;TLG为糖酵解总量;HI为异质性指数;CI为置信区间 -
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