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弥漫大B细胞淋巴瘤(diffuse large B-cell lymphoma,DLBCL)在我国是最常见的一种淋巴瘤类型,其中40%为结外弥漫大B细胞淋巴瘤(extranodal diffuse large B-cell lymphoma,EN-DLBCL)[1]。18F-FDG PET/CT在DLBCL化疗中期时的分期和疗效评估方面的应用价值已被广泛认可,并写入2021年美国国家综合癌症网非霍奇金淋巴瘤治疗指南[2]、中华医学会核医学分会淋巴瘤18F-FDG PET/CT及PET/MR显像临床应用指南(2021版)[3]。但是关于中期PET/CT预测DLBCL疗效和预后的价值,仍存在不少问题有待进一步探讨,例如最佳中期PET/CT时间点难以确定,各种中期PET/CT评估方法的优劣有待对比研究,国际预后指数(international prognosis index,IPI)虽广泛应用于淋巴瘤的预后分层,但在预测高危患者方面仍具有一定的局限性[2, 4-6]。另外,与非EN-DLBCL患者相比,EN-DLBCL患者病情通常更加高危,疗效和预后也更差[6-7],目前罕有以中期18F-FDG PET/CT专门预测EN-DLBCL疗效和预后的研究。本研究对比分析了基于中期18F-FDG PET/CT的几种评估指标在EN-DLBCL患者疗效和预后评估中的价值,以期寻找基于中期18F-FDG PET/CT的最佳评估指标。
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77例EN-DLBCL患者中,明确组织病理学亚型者76例(另外1例组织病理学检查未进行亚型分类),包括生发中心来源30例(39.5%),非生发中心来源46例(60.5%)。IPI评分为低危、中低危、中高危、高危的患者分别为17例(22.1%)、12例(15.6%)、18例(23.4%)、30例(39.0%)。结外病变最常累及的4种脏器分别为脾脏(26例,33.8%)、骨髓(24例,31.2%)、胃(14例,18.2%)、肠(14例,18.2%)。初始化疗结束时,51例(66.2%)患者达到完全缓解、4例(5.2%)死亡,其余患者继续治疗。
患者中位随访时间为24个月,范围为4~105个月。至随访结束时,入组患者中有19例(24.7%)出现疾病进展、复发或死亡,包括11例(14.3%)死亡(其中1例为化疗后因心肌梗死死亡)。患者的一般资料见表1。
一般资料 例数(%) 性别 男 35(45.5) 女 42(54.5) 临床Ann Arbor分期 Ⅰ/Ⅱ期 21(27.3) Ⅲ/Ⅳ期 56(72.7) 初诊LDH水平 升高 41(53.2) 未升高 36(46.8) β2微球蛋白水平 升高 61(79.2) 未升高 16(20.8) 有无B症状 有 26(33.8) 无 51(66.2) ECOG PS评分 0~1分 63(81.8) 2~4分 14(18.2) IPI评分 低危+中低危 29(37.7) 中高危+高危 48(62.3) 结外病变数目 1个 34(44.2) >1个 43(55.8) 重要脏器是否受累 是 50(64.9) 否 27(35.1) Deauville五分法评分 1~3分 40(51.9) 4~5分 37(48.1) Lugano疗效评估 缓解 74(96.1) 未缓解 3(3.9) 初始化疗结束时临床疗效评估 完全缓解 51(66.2) 未完全缓解(部分缓解+疾病稳定或
未缓解+疾病进展,含死亡)26(33.8) 注:LDH为乳酸脱氢酶;ECOG PS为东部肿瘤协作组体能状态评分;IPI为国际预后指数;重要脏器指骨髓、胃、肠、肝或肺 表 1 77例结外弥漫大B细胞淋巴瘤患者的一般资料
Table 1. Clinical characteristics of 77 extranodal diffuse large B-cell lymphoma patients
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ROC曲线结果显示,中期SUVmax的最佳临界值为4.9,因此将患者分为中期SUVmax<4.9组和中期SUVmax≥4.9组。
中期SUVmax<4.9组、Deauville五分法评分1~3分组患者初始化疗结束时的完全缓解率显著高于中期SUVmax≥4.9组(82.6%对41.9%,χ2=13.699,P<0.001)、Deauville五分法评分4~5分组(85.0%对45.9%,χ2=13.108,P<0.001);而以ΔSUVmax 70%、Lugano疗效评估结果分组的各组间完全缓解率的差异均无统计学意义,详见表2。Deauville五分法评分1~3分组的完全缓解率显著高于ΔSUVmax%≥70%组和Lugano疗效评估缓解组,且差异均有统计学意义(χ2=4.130、4.069,P=0.042、0.044);中期SUVmax<4.9组的完全缓解率高于ΔSUVmax%≥70%组和Lugano疗效评估缓解组,但差异均无统计学意义(χ2=3.345、3.282,P=0.067、0.070)。
评估指标 例数 完全缓解(n=51) 未完全缓解(n=26) χ2值 P值 中期SUVmax 中期SUVmax<4.9组 46 38(82.6) 8(17.4) 13.699 <0.001 中期SUVmax≥4.9组 31 13(41.9) 18(58.1) ΔSUVmax70% ΔSUVmax%≥70%组 57 38(66.7) 19(33.3) 0.018 0.892 ΔSUVmax%<70%组 20 13(65.0) 7(35.0) Deauville五分法评分 1~3分组 40 34(85.0) 6(15.0) 13.108 <0.001 4~5分组 37 17(45.9) 20(54.1) Lugano疗效评估 缓解组 74 50(67.6) 24(32.4) 0.368 0.544 未缓解组 3 1(33.3) 2(66.7) 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;EN-DLBCL为结外弥漫大B细胞淋巴瘤;SUVmax为最大标准化摄取值;ΔSUVmax为基线PET与中期PET的SUVmax差值;ΔSUVmax=[(基线SUVmax−中期SUVmax)/基线SUVmax]×100% 表 2 中期18F-FDG PET/CT各评估指标预测EN-DLBCL患者初始化疗结束时疗效的结果分析[例(%)]
Table 2. Results of various evaluation indicators of interm 18F-FDG PET/CT for predicting the efficacy of extranodal diffuse large B-cell lymphoma at the end of primary chemotherapy (case (%))
中期SUVmax<4.9、Deauville五分法评分1~3分预测EN-DLBCL初始化疗结束时疾病完全缓解的灵敏度分别为69.2%和76.9%,特异度分别为74.5%和66.7%,准确率分别为72.7%和70.1%,两指标间的差异均无统计学意义(χ2=0.759、0.391、0.127,均P>0.05)。
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中期SUVmax<4.9组和中期SUVmax≥4.9组的2年PFS率分别为89.0%和60.6%,差异有统计学意义(χ2=6.148,P=0.013);2年OS率分别为92.5%和80.3%,差异无统计学意义(χ2=3.416,P=0.065)。ΔSUVmax%≥70%组和ΔSUVmax%<70%组的2年PFS率分别为79.5%和75.0%,差异无统计学意义(χ2=0.051,P=0.822);2年OS率分别为92.2%和74.4%,差异无统计学意义(χ2=3.331,P=0.068)。Deauville五分法评分1~3分组和4~5分组的2年PFS率分别为89.9%和64.7%,差异有统计学意义(χ2=4.586,P=0.032);2年OS率分别为93.8%和80.8%,差异无统计学意义(χ2=3.447,P=0.063)。Lugano疗效评估缓解组和未缓解组的2年PFS率分别为79.9%和33.3%,差异有统计学意义(χ2=4.765,P=0.029);2年OS率分别为89.7%和33.3%,差异有统计学意义(χ2=7.248,P=0.007)。中期18F-FDG PET/CT各评估指标预测EN-DLBCL的PFS的Kaplan-Meier生存曲线见图1。
图 1 中期18F-FDG PET/CT各评估指标预测77例EN-DLBCL患者PFS的Kaplan-Meier生存曲线
Figure 1. Kaplan-Meier plots of progression free survival in 77 patients with extranodal diffuse large B-cell lymphoma using assessment indicators of interim 18F-FDG PET/CT
EN-DLBCL患者PFS和OS的单因素COX回归分析结果见表3。将表3中P<0.10的评估指标纳入多因素COX回归分析,结果显示Lugano疗效评估、IPI评分是影响EN-DLBCL患者PFS和OS的独立预测指标,详见表4。
影响因素 PFS OS HR(95%CI) P值 HR(95%CI) P值 基线PET/CT 结外病变数目是否>1 4.388(1.409~13.668) 0.011 4.579(0.973~21.545) 0.054 是否有重要脏器受累 3.682(1.062~12.762) 0.040 5.863(0.749~45.896) 0.092 中期PET/CT SUVmax4.9分组 3.052(1.196~7.788) 0.020 3.009(0.877~10.327) 0.080 ΔSUVmax70%分组 0.890(0.319~2.482) 0.823 0.347(0.105~1.147) 0.083 Deauville五分法评分分组 2.737(1.038~7.221) 0.042 3.262(0.864~12.312) 0.081 Lugano疗效评估分组 4.595(1.016~20.783) 0.048 6.293(1.347~29.395) 0.019 初诊时临床特征 是否有B症状 2.609(1.045~6.517) 0.040 1.728(0.526~5.680) 0.368 LDH水平是否升高 4.143(1.365~12.573) 0.012 2.648(0.697~10.064) 0.153 IPI评分分组 7.040(1.611~30.761) 0.009 7.422(0.943~58.388) 0.057 注:EN-DLBCL为结外弥漫大B细胞淋巴瘤;PFS为无进展生存期;OS为总生存期;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;ΔSUVmax为基线PET与中期PET的SUVmax差值;LDH为乳酸脱氢酶;IPI为国际预后指数;HR为风险比;CI为置信区间 表 3 影响EN-DLBCL患者PFS和OS的单因素COX回归分析结果
Table 3. Univariate COX analysis results of progression free survival and overall survival of patients with extranodal diffuse large B-cell lymphoma
影响因素 PFS OS HR(95%CI) P值 HR(95%CI) P值 中期SUVmax4.9分组 2.647(0.992~7.061) 0.052 − − Lugano疗效评估分组 12.179(1.616~91.780) 0.015 8.645(1.768~42.273) 0.008 IPI评分分组 14.330(2.251~91.213) 0.005 8.903(1.089~72.806) 0.041 注:−表示无此项数据;EN-DLBCL为结外弥漫大B细胞淋巴瘤;PFS为无进展生存期;OS为总生存期;SUVmax为最大标准化摄取值;IPI为国际预后指数;HR为风险比;CI为置信区间 表 4 影响EN-DLBCL患者PFS和OS的多因素COX回归分析结果
Table 4. Multivariate COX analysis results of progression free survival and overall survival of patients with extranodal diffuse large B-cell lymphoma
中期18F-FDG PET/CT预测结外弥漫大B细胞淋巴瘤疗效和预后的方法学研究
Methodological study of interim 18F-FDG PET/CT in predicting efficacy and prognosis in patients with extranodal diffuse large B-cell lymphoma
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摘要:
目的 对比分析基于中期18F-氟脱氧葡萄糖(FDG) PET/CT的4项评估指标预测结外弥漫大B细胞淋巴瘤(EN-DLBCL)初始化疗疗效和预后的效能。 方法 回顾性分析2011年5月至2020年4月于北京医院经组织病理学检查或随访结果明确诊断为EN-DLBCL的77例初诊患者[其中,男性35例、女性42例,年龄(62.7±16.2)岁]的资料,包括治疗前基线PET/CT、初始化疗3~4个周期时的中期PET/CT和临床资料,并通过医院电子病历系统或电话随访。采用受试者工作特征(ROC)曲线确定中期PET/CT的最大标准化摄取值(SUVmax)的最佳临界值,将患者分为中期SUVmax<最佳临界值组和中期SUVmax≥最佳临界值组;按照中华医学会核医学分会淋巴瘤18F-FDG PET/CT及PET/MR显像临床应用指南推荐,以ΔSUVmax%=70%为最佳临界值,将患者分为ΔSUVmax%<70%组和ΔSUVmax%≥70%组;根据中期Deauville五分法评分,将患者分为Deauville五分法评分1~3分组和4~5分组;根据Lugano疗效评估标准,以中期疗效将患者分为缓解组和未缓解组。采用χ2检验、Kaplan-Meier生存分析和COX回归分析等方法分析基于中期PET/CT的SUVmax、Deauville五分法评分、Lugano疗效评估结果、ΔSUVmax%等指标对EN-DLBCL初始化疗疗效和预后预测的效能。 结果 (1)初始化疗结束时51例(66.2%)患者完全缓解;中期SUVmax<4.9组、Deauville五分法评分1~3分组的完全缓解率分别为82.6%(38/46)和85.0%(34/40),显著高于对应的其他组,差异均有统计学意义(χ2=13.699、13.108,均P<0.001);以ΔSUVmax70%和Lugano疗效评估结果进行分组的各组,其完全缓解率之间的差异均无统计学意义(χ2=0.018、0.368,均P>0.05)。(2)中位随访时间为24个月,范围为4~105个月,随访结束时19例(24.7%)患者疾病进展、复发或死亡;SUVmax<4.9组、Deauville五分法评分1~3分组、Lugano疗效评估缓解组患者的2年无进展生存期(PFS)均显著优于对应的其他组,差异均有统计学意义(χ2=6.148、4.586、4.765,均P<0.05);Lugano疗效评估缓解组患者的2年总生存期(OS)优于未缓解组,差异有统计学意义(χ2=7.248,P=0.007);以ΔSUVmax70%分组的患者之间的PFS和OS的差异均无统计学意义(χ2=0.051、3.331,均P>0.05)。多因素COX回归分析结果显示,Lugano疗效评估结果、国际预后指数评分是EN-DLBCL患者PFS(HR=12.179、14.330,P=0.015、0.005)和OS(HR=8.645、8.903,P=0.008、0.041)的独立预测指标。 结论 基于EN-DLBCL患者中期18F-FDG PET/CT的4项评估指标中,中期SUVmax<4.9和Deauville五分法评分1~3分能较好地预测EN-DLBCL患者初始化疗结束时的疗效是否为完全缓解,Lugano疗效评估结果是PFS和OS的独立预测指标。 -
关键词:
- 淋巴瘤,大B细胞,弥漫性 /
- 正电子发射断层显像术 /
- 体层摄影术,X线计算机 /
- 预后 /
- 最大标准化摄取值 /
- Deauville五分法 /
- Lugano疗效评估
Abstract:Objective To investigate the predictive accuracies of four indicators based on the interim 18F-fluorodeoxyglucose (FDG) PET/CT in terms of their efficacy and prognoses in patients with extranodal diffuse large B-cell lymphoma (EN-DLBCL). Methods Data of a total of seventy-seven newly diagnosed patients (35 males, 42 females; aged (62.7±16.2) years) with EN-DLBCL confirmed by histopathological examination or follow-up results were retrospectively analyzed from May 2011 to April 2020, including baseline PET/CT before treatment, interim PET/CT during initial chemotherapy for 3 to 4 cycles, and clinical data. Follow-up was performed through the hospital's electronic medical record system or phone call. Using the receiver operating characteristic (ROC) curve to select the optimal cutoff value for interim SUVmax, patients were divided into SUVmax < the cutoff value group and ≥ the cutoff group. Following the clinical practice guideline of 18F-FDG PET/CT and PET/MR in lymphoma (2021 edition), ΔSUVmax=70% was chosen as the cutoff value, patients were divided into ΔSUVmax%<70% group and ≥70% group. Based on the Deauville five-point scale, patients were divided into 1–3 group and 4–5 group. According to the Lugano classification criteria, patients were divided into the disease remission group and unrelieved group based on the interim response evaluation. The χ2 test, Kaplan-Meier, and Cox regression analysis were performed to analyze SUVmax, Deauville five-point scale, and the Lugano classification criteria based on interim PET/CT and ΔSUVmax% between baseline PET and interim PET in order to predict the efficacy of primary chemotherapy and prognosis of EN-DLBCL. Results (1) At the end of primary chemotherapy, 51 patients (66.2%) achieved complete remission (CR). The rates of CR in SUVmax<4.9 group and Deauville scores 1–3 group were 82.6% (38/46) and 85.0% (34/40), respectively, which were significantly higher than those of the other corresponding groups (χ2=13.699, 13.108, both P<0.001). No significant difference was found between the rates of CR of patients grouped by ΔSUVmax70% or the interim response evaluation based on the Lugano classification criteria (χ2=0.018, 0.368, both P>0.05). (2) The median follow-up time was 24 (4–105) months. In addition, 19 patients (24.7%) progressed, relapsed, or died at the end of follow-up. Patients in the SUVmax<4.9 group, Deauville scores 1–3 group, or remission group assessed by the Lugano classification criteria had significantly higher 2-year progression-free survival (PFS) than those in the other corresponding groups (χ2=6.148, 4.586, and 4.765, all P<0.05). The 2-year overall survival (OS) of the remission group was significantly higher than that of the nonremission group (χ2=7.248, P=0.007). No significant difference was found in the PFS or OS between patients grouped by ΔSUVmax70% (χ2=0.051, 3.331, both P>0.05). Furthermore, multivariate COX analysis confirmed that Lugano classification criteria and International Prognosis Index were independent predictors of PFS (HR=12.179, 14.330, P=0.015, 0.005) and OS (HR=8.645, 8.903, P=0.008, 0.041) in EN-DLBCL patients. Conclusion Among the four assessment indicators of interim PET/CT in patients with EN-DLBCL, the interim SUVmax<4.9 and the Deauville scores 1–3 were the better indicators for predicting CR at the end of primary chemotherapy, whereas the interim Lugano classification criteria can be considered an independent predictive factor of PFS and OS. -
表 1 77例结外弥漫大B细胞淋巴瘤患者的一般资料
Table 1. Clinical characteristics of 77 extranodal diffuse large B-cell lymphoma patients
一般资料 例数(%) 性别 男 35(45.5) 女 42(54.5) 临床Ann Arbor分期 Ⅰ/Ⅱ期 21(27.3) Ⅲ/Ⅳ期 56(72.7) 初诊LDH水平 升高 41(53.2) 未升高 36(46.8) β2微球蛋白水平 升高 61(79.2) 未升高 16(20.8) 有无B症状 有 26(33.8) 无 51(66.2) ECOG PS评分 0~1分 63(81.8) 2~4分 14(18.2) IPI评分 低危+中低危 29(37.7) 中高危+高危 48(62.3) 结外病变数目 1个 34(44.2) >1个 43(55.8) 重要脏器是否受累 是 50(64.9) 否 27(35.1) Deauville五分法评分 1~3分 40(51.9) 4~5分 37(48.1) Lugano疗效评估 缓解 74(96.1) 未缓解 3(3.9) 初始化疗结束时临床疗效评估 完全缓解 51(66.2) 未完全缓解(部分缓解+疾病稳定或
未缓解+疾病进展,含死亡)26(33.8) 注:LDH为乳酸脱氢酶;ECOG PS为东部肿瘤协作组体能状态评分;IPI为国际预后指数;重要脏器指骨髓、胃、肠、肝或肺 表 2 中期18F-FDG PET/CT各评估指标预测EN-DLBCL患者初始化疗结束时疗效的结果分析[例(%)]
Table 2. Results of various evaluation indicators of interm 18F-FDG PET/CT for predicting the efficacy of extranodal diffuse large B-cell lymphoma at the end of primary chemotherapy (case (%))
评估指标 例数 完全缓解(n=51) 未完全缓解(n=26) χ2值 P值 中期SUVmax 中期SUVmax<4.9组 46 38(82.6) 8(17.4) 13.699 <0.001 中期SUVmax≥4.9组 31 13(41.9) 18(58.1) ΔSUVmax70% ΔSUVmax%≥70%组 57 38(66.7) 19(33.3) 0.018 0.892 ΔSUVmax%<70%组 20 13(65.0) 7(35.0) Deauville五分法评分 1~3分组 40 34(85.0) 6(15.0) 13.108 <0.001 4~5分组 37 17(45.9) 20(54.1) Lugano疗效评估 缓解组 74 50(67.6) 24(32.4) 0.368 0.544 未缓解组 3 1(33.3) 2(66.7) 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;EN-DLBCL为结外弥漫大B细胞淋巴瘤;SUVmax为最大标准化摄取值;ΔSUVmax为基线PET与中期PET的SUVmax差值;ΔSUVmax=[(基线SUVmax−中期SUVmax)/基线SUVmax]×100% 表 3 影响EN-DLBCL患者PFS和OS的单因素COX回归分析结果
Table 3. Univariate COX analysis results of progression free survival and overall survival of patients with extranodal diffuse large B-cell lymphoma
影响因素 PFS OS HR(95%CI) P值 HR(95%CI) P值 基线PET/CT 结外病变数目是否>1 4.388(1.409~13.668) 0.011 4.579(0.973~21.545) 0.054 是否有重要脏器受累 3.682(1.062~12.762) 0.040 5.863(0.749~45.896) 0.092 中期PET/CT SUVmax4.9分组 3.052(1.196~7.788) 0.020 3.009(0.877~10.327) 0.080 ΔSUVmax70%分组 0.890(0.319~2.482) 0.823 0.347(0.105~1.147) 0.083 Deauville五分法评分分组 2.737(1.038~7.221) 0.042 3.262(0.864~12.312) 0.081 Lugano疗效评估分组 4.595(1.016~20.783) 0.048 6.293(1.347~29.395) 0.019 初诊时临床特征 是否有B症状 2.609(1.045~6.517) 0.040 1.728(0.526~5.680) 0.368 LDH水平是否升高 4.143(1.365~12.573) 0.012 2.648(0.697~10.064) 0.153 IPI评分分组 7.040(1.611~30.761) 0.009 7.422(0.943~58.388) 0.057 注:EN-DLBCL为结外弥漫大B细胞淋巴瘤;PFS为无进展生存期;OS为总生存期;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;ΔSUVmax为基线PET与中期PET的SUVmax差值;LDH为乳酸脱氢酶;IPI为国际预后指数;HR为风险比;CI为置信区间 表 4 影响EN-DLBCL患者PFS和OS的多因素COX回归分析结果
Table 4. Multivariate COX analysis results of progression free survival and overall survival of patients with extranodal diffuse large B-cell lymphoma
影响因素 PFS OS HR(95%CI) P值 HR(95%CI) P值 中期SUVmax4.9分组 2.647(0.992~7.061) 0.052 − − Lugano疗效评估分组 12.179(1.616~91.780) 0.015 8.645(1.768~42.273) 0.008 IPI评分分组 14.330(2.251~91.213) 0.005 8.903(1.089~72.806) 0.041 注:−表示无此项数据;EN-DLBCL为结外弥漫大B细胞淋巴瘤;PFS为无进展生存期;OS为总生存期;SUVmax为最大标准化摄取值;IPI为国际预后指数;HR为风险比;CI为置信区间 -
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