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目前,食管癌位居全球恶性肿瘤死亡原因的第6位[1],其中东亚地区发病率最高。食管鳞状细胞癌(esophageal squamous cell carcinoma,ESCC)占食管癌的90%以上[2],预后较差,且由于发现不及时,50%以上的患者发现时已为中晚期,无法进行手术,放疗和化疗为其主要的治疗方式。美国癌症联合委员会(American Joint Committee on Cancer, AJCC)食管癌TNM 分期对接受放化疗的ESCC患者的指导意义和预测价值有限[3-4],其预后评估主要依靠影像学方法。18F-FDG PET/CT检查作为一种有前景的影像学检查方法而备受关注[5-8],但之前的研究多局限于原发病灶,对淋巴结及远处器官转移灶的研究较少,尤其是对于部分食管癌原发灶肿瘤负荷小,而转移灶肿瘤负荷大的患者,原发灶的代谢参数无法完全反映整体肿瘤负荷。本研究提出了3个比值参数即治疗前转移灶与原发灶的SUVmax、肿瘤代谢体积(metabolic tumor volume,MTV)以及病灶糖酵解总量(total lesion glycolysis,TLG)的比值(the ratio of SUVmax,R-SUVmax)、(the ratio of MTV,R-MTV)、(the ratio of TLG,R-TLG)。本研究回顾性分析放化疗前基线18F-FDG PET/CT代谢参数对ESCC患者预后的预测价值。
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中位随访时间为11个月。至随访结束时,84例(79.2%)患者疾病进展,其中 76例(71.7%)死亡,中位PFS期为9个月(1~63个月),中位OS期为11个月(1~63个月)。
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18F-FDG PET/CT代谢参数预测106例ESCC患者PFS期和OS期的最佳临界值如表1所示。
参数 M(Q1, Q3) 最佳临界值 PFS期 OS期 SUVmax 13.36(9.93, 17.28) 11.2 11.2 MTVp(cm3) 20.58(10.15, 31.36) 55.0 55.0 TLGp(g) 136.90(56.65, 258.89) 434.6 223.2 MTVwb(cm3) 32.08(20.11, 65.11) 130.2 130.2 TLGwb(g) 203.47(102.91, 490.70) 466.5 724.0 R-SUVmax 0.49(0.32, 0.82) 0.7 1.9 R-MTV 0.46(0.15, 1.67) 0.1 0.8 R-TLG 0.20(0.04, 1.05) 3.6 3.6 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;PFS为无进展生存;OS为总生存;SUVmax为最大标准化摄取值;MTVp为原发灶肿瘤代谢体积;TLGp 为原发灶病灶糖酵解总量;MTVwb为全身病灶肿瘤代谢体积;TLGwb为全身病灶糖酵解总量;R-SUVmax 为转移灶与原发灶最大标准化摄取值比值;R-MTV为转移灶与原发灶肿瘤代谢体积比值;R-TLG为转移灶与原发灶病灶糖酵解总量比值 表 1 18F-FDG PET/CT代谢参数预测106例食管鳞状细胞癌 患者PFS期和OS期的最佳临界值
Table 1. The optimal cut-off values of 18F-FDG PET/CT metabolic parameters for predicting progression-free survival and overall survival in 106 patients with esophageal squamous cell carcinoma
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单因素分析结果显示,T分期、MTVp、TLGp、MTVwb、TLGwb、R-TLG是影响接受放化疗ESCC患者PFS期及OS期(均P<0.05)的危险因素(表2,表3);多因素分析结果显示,T分期、R-TLG是影响ESCC患者PFS期(HR=2.210,95%CI:1.307~3.737,P=0.003;HR=3.118,95%CI:1.414~6.875,P=0.005)及OS期(HR=1.885,95%CI:1.072~3.317,P=0.028;HR=2.584,95%CI:1.186~5.629,P=0.017)的独立危险因素(表4)。
临床因素 例数 中位PFS期(月) χ2值 P值 中位OS期(月) χ2值 P值 年龄 2.667 0.102 0.843 0.359 ≤64岁 49 8 12 >64岁 57 10 13 性别 0.001 0.992 0.002 0.965 男 98 9 12 女 8 8 10 原发灶位置 4.374 0.112 5.710 0.058 上段 39 11 17 中段 45 9 12 下段 22 6 10 T分期 11.047 0.001 8.120 0.004 T1~2期 42 16 22 T3~4期 64 6 9 N分期 3.358 0.187 1.538 0.464 N1期 33 8 11 N2期 51 11 12 N3期 22 6 12 M分期 1.493 0.222 1.266 0.261 M0期 92 10 12 M1期 14 6 6 临床分期 0.672 0.412 0.296 0.586 Ⅰ~Ⅲ期 45 11 14 Ⅳ期 61 8 12 分化程度 0.012 0.994 0.611 0.736 低 39 9 15 中 57 9 12 高 10 11 11 治疗方式 3.478 0.176 1.997 0.367 放化疗 67 11 15 单纯放疗 14 8 10 单纯化疗 25 5 9 注:PFS为无进展生存;OS为总生存 表 2 106例食管鳞状细胞癌患者的临床特征及单因素分析
Table 2. Clinical features and univariate analysis of 106 patients with esophageal squamous cell carcinoma
因素 例数 中位PFS期 (月) χ2值 P值 因素 例数 中位OS期 (月) χ2值 P值 原发灶SUVmax 2.943 0.086 原发灶SUVmax 3.225 0.072 ≤11.2 36 14 ≤11.2 36 25 >11.2 70 8 >11.2 70 11 MTVp 10.473 0.001 MTVp 8.703 0.003 ≤55.0 cm3 95 11 ≤55.0 cm3 95 12 >55.0 cm3 11 5 >55.0 cm3 11 6 TLGp 11.138 0.001 TLGp 5.682 0.017 ≤434.6 g 90 11 ≤223.2 g 76 14 >434.6 g 16 4 >223.2 g 30 9 MTVwb 22.117 <0.001 MTVwb 14.361 <0.001 ≤130.2 cm3 95 10 ≤130.2 cm3 95 13 >130.2 cm3 11 3 >130.2 cm3 11 5 TLGwb 27.992 <0.001 TLGwb 11.517 0.001 ≤466.5 g 78 12 ≤724.0 g 92 13 >466.5 g 28 4 >724.0 g 14 5 R-SUVmax 3.199 0.074 R-SUVmax 3.758 0.053 ≤0.7 54 8 ≤1.9 90 11 >0.7 52 11 >1.9 16 25 R-MTV 3.043 0.081 R-MTV 2.247 0.134 ≤0.1 21 8 ≤0.8 64 14 >0.1 85 10 >0.8 42 10 R-TLG 6.804 0.009 R-TLG 4.105 0.043 ≤3.6 94 11 ≤3.6 94 13 >3.6 12 5 >3.6 12 7 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;PFS为无进展生存;OS为总生存;SUVmax为最大标准化摄取值;MTVp为原发灶肿瘤代谢体积;TLGp为原发灶病灶糖酵解总量;MTVwb为全身病灶肿瘤代谢体积;TLGwb为全身病灶糖酵解总量;R-SUVmax 为转移灶与原发灶最大标准化摄取值比值;R-MTV为转移灶与原发灶肿瘤代谢体积比值;R-TLG为转移灶与原发灶病灶糖酵解总量比值 表 3 18F-FDG PET/CT代谢参数预测106例食管鳞状细胞癌患者PFS期和OS期的单因素分析
Table 3. Univariate analysis of 18F-FDG PET/CT metabolic parameters for predicting progression-free survival and overall survival in 106 patients with esophageal squamous cell carcinoma
因素 PFS期 OS期 β值 Wald值 P值 HR(95%CI) β值 Wald值 P值 HR(95%CI) T分期 0.793 8.762 0.003 2.210(1.307~3.737) 0.634 4.842 0.028 1.885(1.072~3.317) MTVp −0.004 0.001 0.994 0.996(0.315~3.143) 0.424 0.708 0.400 1.528(0.569~4.102) TLGp 0.521 1.390 0.238 1.683(0.708~4.000) 0.232 0.517 0.472 1.261(0.671~2.370) MTVwb 0.715 2.317 0.128 2.045(0.814~5.136) 0.372 0.609 0.435 1.451(0.570~3.692) R-TLG 1.137 7.946 0.005 3.118(1.414~6.875) 0.949 5.711 0.017 2.584(1.186~5.629) 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;PFS为无进展生存;OS为总生存;MTVp为原发灶肿瘤代谢体积;TLGp 为原发灶病灶糖酵解总量;MTVwb为全身病灶肿瘤代谢体积;R-TLG为转移灶与原发灶病灶糖酵解总量比值 表 4 106例食管鳞状细胞癌患者PFS期和OS期的多因素分析
Table 4. Multivariate analysis for predicting progression-free survival and overall survival in 106 patients with esophageal squamous cell carcinoma
联合T分期及R-TLG将患者分为3组:低 R-TLG且T1~2期为低危组 (n=34)、高R-TLG或T3~4期为中危组(n=68)、高R-TLG且T3~4期为高危组(n=4),结果显示,各组患者间PFS期及OS期的差异均有统计学意义(χ2=38.392、19.857,均P<0.001)(图1)。T分期越高、R-TLG越大,ESCC患者生存期越短,预后越差。典型病例见图2~3。
图 1 18F-FDG PET/CT 代谢参数R-TLG联合T分期预测106例食管鳞状细胞癌患者PFS期(A)和OS期(B)预后的Kaplan-Meier生存曲线
Figure 1. Kaplan-Meier survival curves for progression-free survival and overall survival of 106 patients with esophageal squamous cell carcinoma according to 18F-FDG PET/CT metabolic parameter R-TLG combined with T stage
基线18F-FDG PET/CT代谢参数对伴有转移的食管鳞状细胞癌放化疗患者预后的预测价值
Prognostic value of baseline 18F-FDG PET/CT metabolic parameters in the prognosis of patients with metastasis esophageal squamous cell carcinoma with chemoradiotherapy
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摘要:
目的 探究治疗前18F-氟脱氧葡萄糖(FDG) PET/CT显像原发灶与转移灶代谢参数对接受放化疗的食管鳞状细胞癌(ESCC)患者预后的预测价值。 方法 回顾性分析2013年11月至2021年4月于青岛大学附属医院行18F-FDG PET/CT检查的106例接受放化疗的ESCC患者的临床资料,其中男性98例、女性8例,年龄(63.9±8.8)岁。临床因素包括年龄、性别、原发灶位置、临床分期、分化程度和治疗方式。以40%最大标准化摄取值(SUVmax)作为阈值,勾画治疗前食管癌原发病灶及转移灶的感兴趣区(ROI),获得相应的食管癌原发灶的SUVmax,原发灶的肿瘤代谢体积(MTVp),原发灶的病灶糖酵解总量(TLGp)和全身病灶的MTV(MTVwb),全身病灶的TLG(TLGwb),转移灶与原发灶SUVmax,MTV,TLG的比值(R-SUVmax、R-MTV、R-TLG)。采用Kaplan-Meier法及Log-Rank检验进行单因素分析,采用Cox比例风险模型进行多因素分析,预测影响患者无进展生存(PFS)期及总生存(OS)期的预后因素。 结果 单因素分析结果显示,T分期、MTVp、TLGp、MTVwb、TLGwb及R-TLG是影响接受放化疗ESCC患者PFS期和OS期的危险因素(χ2=4.105~27.992,均P<0.05);多因素分析结果显示,T分期及R-TLG为ESCC患者PFS期(HR=2.210,95%CI:1.307~3.737,P=0.003;HR=3.118,95%CI:1.414~6.875,P=0.005)及OS期(HR=1.885,95%CI:1.072~3.317,P=0.028;HR=2.584,95%CI:1.186~5.629;P=0.017)的独立预后因素。联合T分期及R-TLG将患者分为低、中、高危3组,结果显示,各组患者间PFS期及OS期的差异均有统计学意义(χ2=38.392、19.857,均P<0.001)。 结论 ESCC患者放化疗前T分期和18F-FDG PET/CT代谢参数R-TLG为PFS期及OS期的独立预后因素。 -
关键词:
- 食管肿瘤 /
- 癌,鳞状细胞 /
- 正电子发射断层显像术 /
- 体层摄影术,X线计算机 /
- 氟脱氧葡萄糖F18 /
- 预后
Abstract:Objective To investigate the prognostic value of primary and metastatic metabolic parameters of 18F-fluorodeoxyglucose(FDG) PET/CT imaging before chemoradiotherapy in patients with esophageal squamous cell carcinoma (ESCC). Methods A retrospective analysis was performed on 106 patients [98 males, 8 females, aged (63.9±8.8) years] with metastatic ESCC who received radiochemotherapy and underwent 18F-FDG PET/CT from November 2013 to April 2021 in the Affiliated Hospital of Qingdao University. Clinical factors included age, sex, primary location, clinical stage, degree of differentiation, and treatment. Using 40% maximum standardized uptake value (SUVmax) as the threshold, delineate the region of interest (ROI) of the primary and metastatic lesions of esophageal cancer before treatment. Metabolic parameters included SUVmax of primary lesion, metabolic tumor volume (MTV) of primary lesion (MTVp), total lesion glycolysis (TLG) of primary lesion (TLGp), MTV of whole body (MTVwb), TLG of whole body (TLGwb), and SUVmax, MTV, TLG ratio of metastatic lesion to primary lesion (R-SUVmax, R-MTV, R-TLG). Kaplan-Meier method and Log-Rank test were used for univariate analysis and multivariate analysis was conducted by Cox proportional hazards model to predict the prognostic factors affecting progression-free survival (PFS) and overall survival (OS) of patients. Results Univariate analysis showed that T stage, MTVp, TLGp, MTVwb, TLGwb and R-TLG were prognostic factors for PFS and OS in ESCC patients receiving chemoradiotherapy (χ2=4.105−27.992, all P<0.05). Multivariate analysis showed that T stage and R-TLG were independent prognostic factors for PFS (HR=2.210, 95%CI: 1.307−3.737, P=0.003; HR=3.118, 95%CI: 1.414−6.875, P=0.005) and OS (HR=1.885, 95%CI: 1.072−3.317, P=0.028; HR=2.584, 95%CI: 1.186−5.629, P=0.017) in ESCC patients. Combined with T stage and R-TLG, the patients were divided into low-risk, medium-risk and high-risk groups. The results showed that there were statistically significant differences in PFS and OS among the groups (χ2=38.392, 19.857; both P<0.001). Conclusion T stage and 18F-FDG PET/CT metabolic parameter R-TLG were independent prognostic factors for PFS and OS in ESCC patients before chemoradiotherapy. -
图 1 18F-FDG PET/CT 代谢参数R-TLG联合T分期预测106例食管鳞状细胞癌患者PFS期(A)和OS期(B)预后的Kaplan-Meier生存曲线
Figure 1. Kaplan-Meier survival curves for progression-free survival and overall survival of 106 patients with esophageal squamous cell carcinoma according to 18F-FDG PET/CT metabolic parameter R-TLG combined with T stage
表 1 18F-FDG PET/CT代谢参数预测106例食管鳞状细胞癌 患者PFS期和OS期的最佳临界值
Table 1. The optimal cut-off values of 18F-FDG PET/CT metabolic parameters for predicting progression-free survival and overall survival in 106 patients with esophageal squamous cell carcinoma
参数 M(Q1, Q3) 最佳临界值 PFS期 OS期 SUVmax 13.36(9.93, 17.28) 11.2 11.2 MTVp(cm3) 20.58(10.15, 31.36) 55.0 55.0 TLGp(g) 136.90(56.65, 258.89) 434.6 223.2 MTVwb(cm3) 32.08(20.11, 65.11) 130.2 130.2 TLGwb(g) 203.47(102.91, 490.70) 466.5 724.0 R-SUVmax 0.49(0.32, 0.82) 0.7 1.9 R-MTV 0.46(0.15, 1.67) 0.1 0.8 R-TLG 0.20(0.04, 1.05) 3.6 3.6 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;PFS为无进展生存;OS为总生存;SUVmax为最大标准化摄取值;MTVp为原发灶肿瘤代谢体积;TLGp 为原发灶病灶糖酵解总量;MTVwb为全身病灶肿瘤代谢体积;TLGwb为全身病灶糖酵解总量;R-SUVmax 为转移灶与原发灶最大标准化摄取值比值;R-MTV为转移灶与原发灶肿瘤代谢体积比值;R-TLG为转移灶与原发灶病灶糖酵解总量比值 表 2 106例食管鳞状细胞癌患者的临床特征及单因素分析
Table 2. Clinical features and univariate analysis of 106 patients with esophageal squamous cell carcinoma
临床因素 例数 中位PFS期(月) χ2值 P值 中位OS期(月) χ2值 P值 年龄 2.667 0.102 0.843 0.359 ≤64岁 49 8 12 >64岁 57 10 13 性别 0.001 0.992 0.002 0.965 男 98 9 12 女 8 8 10 原发灶位置 4.374 0.112 5.710 0.058 上段 39 11 17 中段 45 9 12 下段 22 6 10 T分期 11.047 0.001 8.120 0.004 T1~2期 42 16 22 T3~4期 64 6 9 N分期 3.358 0.187 1.538 0.464 N1期 33 8 11 N2期 51 11 12 N3期 22 6 12 M分期 1.493 0.222 1.266 0.261 M0期 92 10 12 M1期 14 6 6 临床分期 0.672 0.412 0.296 0.586 Ⅰ~Ⅲ期 45 11 14 Ⅳ期 61 8 12 分化程度 0.012 0.994 0.611 0.736 低 39 9 15 中 57 9 12 高 10 11 11 治疗方式 3.478 0.176 1.997 0.367 放化疗 67 11 15 单纯放疗 14 8 10 单纯化疗 25 5 9 注:PFS为无进展生存;OS为总生存 表 3 18F-FDG PET/CT代谢参数预测106例食管鳞状细胞癌患者PFS期和OS期的单因素分析
Table 3. Univariate analysis of 18F-FDG PET/CT metabolic parameters for predicting progression-free survival and overall survival in 106 patients with esophageal squamous cell carcinoma
因素 例数 中位PFS期 (月) χ2值 P值 因素 例数 中位OS期 (月) χ2值 P值 原发灶SUVmax 2.943 0.086 原发灶SUVmax 3.225 0.072 ≤11.2 36 14 ≤11.2 36 25 >11.2 70 8 >11.2 70 11 MTVp 10.473 0.001 MTVp 8.703 0.003 ≤55.0 cm3 95 11 ≤55.0 cm3 95 12 >55.0 cm3 11 5 >55.0 cm3 11 6 TLGp 11.138 0.001 TLGp 5.682 0.017 ≤434.6 g 90 11 ≤223.2 g 76 14 >434.6 g 16 4 >223.2 g 30 9 MTVwb 22.117 <0.001 MTVwb 14.361 <0.001 ≤130.2 cm3 95 10 ≤130.2 cm3 95 13 >130.2 cm3 11 3 >130.2 cm3 11 5 TLGwb 27.992 <0.001 TLGwb 11.517 0.001 ≤466.5 g 78 12 ≤724.0 g 92 13 >466.5 g 28 4 >724.0 g 14 5 R-SUVmax 3.199 0.074 R-SUVmax 3.758 0.053 ≤0.7 54 8 ≤1.9 90 11 >0.7 52 11 >1.9 16 25 R-MTV 3.043 0.081 R-MTV 2.247 0.134 ≤0.1 21 8 ≤0.8 64 14 >0.1 85 10 >0.8 42 10 R-TLG 6.804 0.009 R-TLG 4.105 0.043 ≤3.6 94 11 ≤3.6 94 13 >3.6 12 5 >3.6 12 7 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;PFS为无进展生存;OS为总生存;SUVmax为最大标准化摄取值;MTVp为原发灶肿瘤代谢体积;TLGp为原发灶病灶糖酵解总量;MTVwb为全身病灶肿瘤代谢体积;TLGwb为全身病灶糖酵解总量;R-SUVmax 为转移灶与原发灶最大标准化摄取值比值;R-MTV为转移灶与原发灶肿瘤代谢体积比值;R-TLG为转移灶与原发灶病灶糖酵解总量比值 表 4 106例食管鳞状细胞癌患者PFS期和OS期的多因素分析
Table 4. Multivariate analysis for predicting progression-free survival and overall survival in 106 patients with esophageal squamous cell carcinoma
因素 PFS期 OS期 β值 Wald值 P值 HR(95%CI) β值 Wald值 P值 HR(95%CI) T分期 0.793 8.762 0.003 2.210(1.307~3.737) 0.634 4.842 0.028 1.885(1.072~3.317) MTVp −0.004 0.001 0.994 0.996(0.315~3.143) 0.424 0.708 0.400 1.528(0.569~4.102) TLGp 0.521 1.390 0.238 1.683(0.708~4.000) 0.232 0.517 0.472 1.261(0.671~2.370) MTVwb 0.715 2.317 0.128 2.045(0.814~5.136) 0.372 0.609 0.435 1.451(0.570~3.692) R-TLG 1.137 7.946 0.005 3.118(1.414~6.875) 0.949 5.711 0.017 2.584(1.186~5.629) 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;PFS为无进展生存;OS为总生存;MTVp为原发灶肿瘤代谢体积;TLGp 为原发灶病灶糖酵解总量;MTVwb为全身病灶肿瘤代谢体积;R-TLG为转移灶与原发灶病灶糖酵解总量比值 -
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