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非霍奇金淋巴瘤(non-Hodgkin's lymphoma,NHL)是一种起源于淋巴组织细胞,具有较强异质性的恶性肿瘤。NHL的治疗方法以综合治疗为主,如化疗、靶向治疗和免疫治疗。自体造血干细胞移植(autologous hematopoietic stem cell transplantation,ASCT)在NHL患者的治疗中也占据重要地位,美国国立综合癌症网络(National Comprehensive Cancer Network,NCCN)指南(第3版)指出,ASCT可作为一线诱导化疗后的巩固治疗应用于中-高危、高危NHL患者[1],同时,ASCT也适用于复发后对化疗敏感的NHL患者的挽救治疗[2-3]。NHL患者ASCT后的预后评估可以筛选出在ASCT后早期需要选择更适合的治疗方案(如放疗、放射免疫治疗、异基因干细胞移植等)的患者,使预后良好的患者避免接受过度治疗。
18F-FDG PET/CT在血液系统恶性肿瘤预后评估中的价值已经被证实,临床上已用于大多数淋巴瘤的分期、再分期和治疗反应的评估[4-7]。目前,18F-FDG PET/CT对淋巴瘤患者ASCT疗效评价的研究多根据Deauville评分(Deauvile score,DS)或Lugano标准进行[8-11]。2017 国际工作组共识认为淋巴瘤疗效评价标准(response evaluation criteria in lymphoma, RECIL)作为新的疗效评价标准正在临床逐渐得到应用[12]。RECIL基于18F-FDG PET/CT的代谢改变和CT的影像学改变,增加了轻微缓解(minor response,MiR)这一类别,对于疗效的评价更细化,有助于指导临床选择精准的治疗方案及在治疗过程中及时调整治疗方案。截至目前,国内鲜有研究分析RECIL在ASCT后NHL患者预后评估中的价值。本研究探讨了RECIL在NHL患者ASCT后预后评估中的价值,并与Lugano标准进行对比研究。
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86例NHL患者临床资料的比较见表1。有效组与无效组患者ASCT后病灶SUVmax、移植前化疗方案数和移植时机的差异均有统计学意义(均P<0.05),性别、年龄、移植前病灶SUVmax、Ann Arbor分期、结外受累数目、组织病理学类型、ECOG 评分和aaIPI评分的差异均无统计学意义(均P>0.05)(表1)。
项目 有效组(n=67) 无效组(n=19) 检验值 P值 性别(例,%) χ2=0.403 0.525 男 48(71.6) 15(78.9) 女 19(28.4) 4(21.1) 年龄(例,%) χ2=0.100 0.752 ≤35岁 38(56.7) 10(52.6) >35岁 29(43.3) 9(47.4) 移植前病灶SUVmax[M(Q1,Q2)] 1.6(1.1,2.2) 1.3(1.0,1.5) Z=−1.702 0.089 移植后病灶SUVmax[M(Q1,Q2)] 1.3(1.0,2.0) 5.2(4.8,8.9) Z=−6.149 <0.001 Ann Arbor分期(例,%) χ2=1.780 0.182 Ⅰ~Ⅱ 21(31.3) 3(15.8) Ⅲ~Ⅳ 46(68.7) 16(84.2) 结外受累数目(例,%) χ2=0.304 0.581 ≥2 27(40.3) 9(47.4) <2 40(59.7) 10(52.6) 组织病理学类型(例,%) χ2=4.035 0.127 DLBCL 30(44.8) 4(21.1) NKTCL 16(23.9) 5(26.3) 其他类型 21(31.3) 10(52.6) ECOG 评分(例,%) χ2=2.054 0.152 <2分 41(61.2) 15(78.9) ≥2分 26(38.8) 4(21.1) aaIPI评分(例,%) χ2=0.367 0.545 <2分 30(44.8) 10(52.6) ≥2分 37(55.2) 9(47.4) 移植前化疗方案数(例,%) χ2=11.949 <0.001 <2 44(65.7) 4(21.1) ≥2 23(34.3) 15(78.9) 移植时机(例,%) χ2=19.897 <0.001 挽救治疗组 11(16.4) 13(68.4) 一线巩固治疗组 56(83.6) 6(31.6) 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;RECIL为淋巴瘤疗效评价标准;SUVmax为最大标准化摄取值;DLBCL为弥漫大B细胞淋巴瘤;NKTCL为自然杀伤/T细胞性淋巴瘤;ECOG为东部肿瘤协作组体能状态;aaIPI为以年龄调整的国际预后指数 表 1 86例行自体造血干细胞移植的非霍奇金淋巴瘤患者的临床资料和18F-FDG PET/CT参数与RECIL疗效评估的关系
Table 1. The relationship between clinical data,18F-FDG PET/CT parameters of 86 patients with non-Hodgkin's lymphoma after autologous hematopoietic stem cell transplantation and the evaluation of response evaluation criteria in lymphoma efficacy
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单因素Cox比例风险回归分析结果表明,移植后SUVmax、RECIL、移植前化疗方案数和移植时机是ASCT后NHL患者预后的影响因素(均P<0.05)(表2)。将RECIL、移植后SUVmax、移植前化疗方案数和移植时机纳入多因素Cox比例风险回归分析,结果显示RECIL是影响ASCT后NHL患者预后的独立危险因素(P<0.05)(表3)。
因素 HR值 95%CI P值 性别 1.587 0.343~7.350 0.555 年龄 1.035 0.991~1.080 0.119 移植前SUVmax 0.896 0.466~1.722 0.741 移植后SUVmax 1.177 1.087~1.274 <0.001 Ann Arbor分期 0.227 0.029~1.775 0.158 组织病理学类型 1.544 0.764~3.121 0.226 结外受累数目 1.158 0.339~3.962 0.815 ECOG 评分 5.932 0.759~46.377 0.090 aaIPI 评分 1.969 0.576~6.731 0.280 RECIL 0.020 0.003~0.155 <0.001 移植前化疗方案数 6.197 1.338~28.711 0.020 移植时机 8.808 2.289~33.891 0.002 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;RECIL为淋巴瘤疗效评价标准;SUVmax为最大标准化摄取值;ECOG为东部肿瘤协作组体能状态;aaIPI为以年龄调整的国际预后指数;HR为风险比;CI为置信区间 表 2 行自体造血干细胞移植的非霍奇金淋巴瘤患者的临床特征、18F-FDG PET/CT参数、RECIL与3年总生存率关系的单因素Cox比例风险回归分析
Table 2. Univariate Cox proportional risk regression analysis of the relationship between clinical features, 18F-FDG PET/CT parameters, response evaluation criteria in lymphoma and 3-year overall survival rate in patients with non-Hodgkin's lymphoma undergoing autologous hematopoietic stem cell transplantation
因素 HR值 95%CI P值 RECIL 0.040 0.004~0.439 0.008 移植后SUVmax 1.039 0.877~1.229 0.660 移植前化疗方案数 2.108 0.307~14.477 0.448 移植时机 1.756 0.382~8.081 0.469 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;RECIL为淋巴瘤疗效评价标准;SUVmax为最大标准化摄取值;HR为风险比;CI为置信区间 表 3 行自体造血干细胞移植的非霍奇金淋巴瘤患者的临床特征、18F-FDG PET/CT参数、RECIL与3年总生存率关系的多因素Cox比例风险回归分析
Table 3. Multivariate Cox proportional risk regression analysis of the relationship between clinical features, 18F-FDG PET/CT parameters, response evaluation criteria in lymphoma and 3-year overall survival rate in patients with non-Hodgkin's lymphoma undergoing autologous hematopoietic stem cell transplantation
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依据Lugano标准,CR患者 49例(57.0%,49/86)、PR 15例(17.4%,15/86)、SD 8例(9.3%,8/86)、PD 14例(16.3%,14/86);依据RECIL,将MiR患者纳入PR,则CR患者 49例(57.0%,49/86)、PR 18例(20.9%,18/86)、SD 2例(2.3%,2/86)、PD 17例(19.8%,17/86)。其中1例NKTCL患者(图1)依据RECIL评估为MiR,依据Lugano标准评估为CR。RECIL与Lugano标准对NHL患者ASCT后疗效评价的结果具有较好的一致性[86.0%(74/86),Kappa=0.77,P<0.001]。 -
依据RECIL,将CR患者纳入完全缓解组,PR+MiR患者纳入部分缓解组,SD+PD患者纳入无效组。依据Lugano标准,将CR患者纳入完全缓解组,PR患者纳入部分缓解组,SD+PD患者纳入无效组。Kaplan-Meier生存分析结果显示,RECIL预测完全缓解组、部分缓解组、无效组患者3年OS率[2.0%(1/49) 对0(0/18)对52.6%(10/19)]的差异与Lugano标准预测3组患者3年OS率[2.0%(1/49)对0(0/15)对45.5%(10/22)]的差异均有统计学意义(χ2=42.727、33.646,均P<0.001)(图2)。
图 2 淋巴瘤疗效评价标准(A)和Lugano标准(B)预测86例非霍奇金淋巴瘤患者自体造血干细胞移植后3年总生存率的Kaplan-Meier生存曲线
Figure 2. Kaplan-Meier survival curve for predicting the 3-year overall survival rate of 86 non-Hodgkin's lymphoma patients after autologous hematopoietic stem cell transplantation using the response evaluation criteria in lymphoma (A) and Lugano criteria (B)
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在预测预后的ROC曲线中,RECIL的AUC为0.884(95%CI:0.763~1.000,P<0.001),Lugano标准的AUC为0.865(95%CI:0.745~0.986,P<0.001);RECIL的AUC略高于Lugano标准,二者的差异无统计学意义(Z=1.334,P>0.05)(图3)。
图 3 淋巴瘤疗效评价标准与Lugano标准预测86例自体造血干细胞移植后非霍奇金淋巴瘤患者预后的受试者工作特征曲线
Figure 3. Receiver operating characteristic curve for predicting prognosis of 86 patients with non-Hodgkin's lymphoma after autologous hematopoietic stem cell transplantation by response evaluation criteria in lymphoma standard and Lugano standard
RECIL对NHL患者自体造血干细胞移植后的预后评估及与Lugano标准的对比研究
Prognostic evaluation of NHL patients after autologous hematopoietic stem cell transplantation using RECIL and comparative study with Lugano standard
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摘要:
目的 探讨自体造血干细胞移植(ASCT)后18F-氟脱氧葡萄糖(FDG)PET/CT显像淋巴瘤疗效评价标准(RECIL)对非霍奇金淋巴瘤(NHL)患者预后评估的价值并与Lugano标准进行对比研究。 方法 回顾性分析2010年10月至2021年11月于山西省肿瘤医院经组织病理学检查结果确诊的86例NHL患者的临床资料和影像资料,其中男性63例、女性23例,年龄34.0(22.0,47.0)岁。所有患者均在ASCT前后行18F-FDG PET/CT显像。根据RECIL在ASCT后对所有患者进行疗效评价,依据患者疗效评价结果将患者分为有效组:完全缓解(CR)、部分缓解(PR)、轻微缓解(MiR);无效组:疾病稳定(SD)、疾病进展(PD)。依据Lugano标准在ASCT后对所有患者进行疗效评价,将患者分为完全缓解组(CR)、部分缓解组(PR)、无效组(SD+PD);依据RECIL将患者分为:完全缓解组(CR)、部分缓解组(PR+MiR)、无效组(SD+PD),随访分析患者3年总生存(OS)期情况。采用卡方检验或Mann-Whitney U检验比较有效组和无效组患者的临床特征和18F-FDG PET/CT参数的差异;采用单因素及多因素Cox比例风险回归分析筛选影响ASCT后NHL患者预后的相关因素;采用Kappa检验评价RECIL和Lugano标准评估NHL患者ASCT后疗效的一致性;采用Kaplan-Meier生存分析比较RECIL与Lugano标准完全缓解组、部分缓解组和无效组间3年OS率的差异;采用Log-rank检验分析3组间3年OS率的差异;采用ROC曲线比较RECIL及Lugano标准对NHL患者ASCT后3年OS率的预测效能。 结果 有效组与无效组患者ASCT后SUVmax[1.3(1.0,2.0)对5.2(4.8,8.9)]的差异有统计学意义(Z=−6.149,P<0.001),有效组移植前化疗方案数<2次的患者占比[65.7%(44/67)]高于无效组[21.1%(4/19)],且差异有统计学意义(χ2=11.949,P<0.001);有效组一线巩固治疗组的患者占比[83.6%(56/67)]高于无效组[31.6%(6/19)],差异有统计学意义(χ2=19.897,P<0.001)。单因素Cox比例风险回归分析结果显示,RECIL(HR=0.020,95%CI:0.003~0.155,P<0.001)、移植后SUVmax(HR=1.177,95%CI:1.087~1.274,P<0.001)、移植前化疗方案数(HR=6.197,95%CI:1.338~28.711,P<0.05)和移植时机(HR=8.808,95%CI:2.289~33.891,P<0.01)是NHL患者预后的影响因素。多因素Cox比例风险回归分析结果显示,RECIL是NHL患者预后的独立危险因素(HR=0.040,95%CI:0.004~0.439,P<0.01)。RECIL与Lugano标准对NHL患者ASCT后的疗效评价具有较好的一致性[86.0%(74/86),Kappa=0.77,P<0.001]。Kaplan-Meier生存分析结果显示,RECIL与Lugano标准的完全缓解组、部分缓解组和无效组3年OS率[2.0%(1/49)对0(0/18)对52.0(10/19),2.0%(1/49)对0(0/15)对45.5%(10/22)]的差异均有统计学意义(χ2=42.727、33.646,均P<0.001)。RECIL预测3年OS率的曲线下面积(AUC)略高于Lugnao标准的AUC(0.884对0.865,Z=1.334,P>0.05)。 结论 ASCT后RECIL可以准确评估NHL患者的预后,RECIL与Lugano标准对NHL患者ASCT后的预后评价作用接近。 -
关键词:
- 淋巴瘤,非霍奇金 /
- 氟脱氧葡萄糖F18 /
- 正电子发射断层显像术 /
- 体层摄影术,X线计算机 /
- 自体造血干细胞移植 /
- RECIL /
- Lugnao标准
Abstract:Objective To explore the prognostic evaluation of the 18F-FDG PET/CT imaging response evaluation criteria in lymphoma (RECIL) for patients with non-Hodgkin's lymphoma (NHL) after autologous hematopoietic stem cell transplantation (ASCT) and compares it with the Lugano standard. Methods The clinical data and imaging data of 86 patients with NHL diagnosed by histopathological examination in Shanxi Provincial Cancer Hospital from October 2010 to November 2021 were retrospectively analyzed, including 63 male and 23 female, aged 34.0(22.0, 47.0) years old. All patients underwent 18F-FDG PET/CT imaging before and after ASCT. According to the RECIL, all patients were evaluated for efficacy after ASCT. Based on the results of the patient efficacy evaluation, patients were divided into effective groups: complete remission (CR), partial remission (PR), and minor remission (MiR), and invalid groups: stable disease(SD), and progressive disease(PD). According to the Lugano standard, the patients were divided into complete remission group (CR), partial remission group (PR), and ineffective group (SD+PD). According to the RECIL, the patients were divided into complete remission group (CR), partial remission group (PR+MiR), andineffective group (SD+PD). The three-year overall survival (OS) period of the patients was followed up and analyzed. Pearson Chi-squared test and Mann Whitney U test were used to compare the differences in clinical features and the 18F-FDG PET/CT parameters between the effective group and the ineffective group. Univariate and multivariate Cox proportional risk regression analysis were used to screen for relevant factors affecting the prognosis of patients with NHL after ASCT. Kappa test was used to evaluate the consistency of efficacy between the RECIL and Lugano standard in evaluating the efficacy of ASCT in patients with NHL. Kaplan-Meier survival analysis was used to compare the differences in three-year OS rates between RECIL and Lugano standard in complete remission, partial remission, and ineffective groups. Log rank test was used to analyze the differences in three-year OS rates among the three groups. ROC curves were used to compare the predictiveefficacy of the RECIL and Lugano standard in three-year OS rates. Results A statistically significant difference was observed in SUVmax (1.3(1.0, 2.0) vs. 5.2(4.8, 8.9)) between the effective group and the ineffective group after transplantation (Z=−6.149, P<0.001). The percentage of patients in the effective group who received less than two chemotherapy regimens before transplantation (65.7%(44/67)) was higher than those in the ineffective group (21.1%(4/19)), and the difference was statistically significant (χ2=11.949, P<0.001). The percentage of patients in the first-line consolidation treatment group (83.6% (56/67)) was higher than those in the ineffective group (31.6%(6/19)), and the difference was statistically significant (χ2=19.897, P<0.001). The results of univariate Cox proportional risk regression analysis showed the RECIL (HR=0.020, 95%CI: 0.003–0.155, P<0.001), post-transplant SUVmax (HR=1.177, 95%CI: 1.087–1.274, P<0.001), number of pretransplant chemotherapy regimens (HR=6.197, 95%CI: 1.338–28.711, P<0.05), and transplant timing (HR=8.808, 95%CI: 2.289–33.891, P<0.01) were prognostic factors for patients with NHL. The results of multivariate Cox proportional risk regression analysis showed the RECIL (HR=0.040, 95%CI: 0.004–0.439, P<0.01) was an independent risk factor for the prognosis of patients with NHL. The RECIL and Lugano standard were consistent in the efficacy evaluation of patients with NHL after ASCT (86.0%(74/86), Kappa=0.77, P<0.001). The Kaplan-Meier survival analysis results showed statistically significantdifferences in three-year OS rates (2.2%(1/49) vs. 0(0/18) vs. 52.0%(10/19), 2.2%(1/49) vs. 0(0/15) vs. 45.5%(10/22)) between the complete remission group, partial remission group, and ineffective group according to the RECIL and Lugano standard (χ2=42.727, 33.646; both P<0.001). The area under curve predicted by the RECIL for the three-year OS rate was slightly higher than that of the Lugano standard (0.884 vs. 0.865, Z=1.334, P>0.05). Conclusion The RECIL can accurately evaluate the prognosis of patients with NHL after ASCT, and the RECIL and Lugano standard have similar prognostic evaluation effects on patients with NHL after ASCT. -
图 2 淋巴瘤疗效评价标准(A)和Lugano标准(B)预测86例非霍奇金淋巴瘤患者自体造血干细胞移植后3年总生存率的Kaplan-Meier生存曲线
Figure 2. Kaplan-Meier survival curve for predicting the 3-year overall survival rate of 86 non-Hodgkin's lymphoma patients after autologous hematopoietic stem cell transplantation using the response evaluation criteria in lymphoma (A) and Lugano criteria (B)
图 3 淋巴瘤疗效评价标准与Lugano标准预测86例自体造血干细胞移植后非霍奇金淋巴瘤患者预后的受试者工作特征曲线
Figure 3. Receiver operating characteristic curve for predicting prognosis of 86 patients with non-Hodgkin's lymphoma after autologous hematopoietic stem cell transplantation by response evaluation criteria in lymphoma standard and Lugano standard
表 1 86例行自体造血干细胞移植的非霍奇金淋巴瘤患者的临床资料和18F-FDG PET/CT参数与RECIL疗效评估的关系
Table 1. The relationship between clinical data,18F-FDG PET/CT parameters of 86 patients with non-Hodgkin's lymphoma after autologous hematopoietic stem cell transplantation and the evaluation of response evaluation criteria in lymphoma efficacy
项目 有效组(n=67) 无效组(n=19) 检验值 P值 性别(例,%) χ2=0.403 0.525 男 48(71.6) 15(78.9) 女 19(28.4) 4(21.1) 年龄(例,%) χ2=0.100 0.752 ≤35岁 38(56.7) 10(52.6) >35岁 29(43.3) 9(47.4) 移植前病灶SUVmax[M(Q1,Q2)] 1.6(1.1,2.2) 1.3(1.0,1.5) Z=−1.702 0.089 移植后病灶SUVmax[M(Q1,Q2)] 1.3(1.0,2.0) 5.2(4.8,8.9) Z=−6.149 <0.001 Ann Arbor分期(例,%) χ2=1.780 0.182 Ⅰ~Ⅱ 21(31.3) 3(15.8) Ⅲ~Ⅳ 46(68.7) 16(84.2) 结外受累数目(例,%) χ2=0.304 0.581 ≥2 27(40.3) 9(47.4) <2 40(59.7) 10(52.6) 组织病理学类型(例,%) χ2=4.035 0.127 DLBCL 30(44.8) 4(21.1) NKTCL 16(23.9) 5(26.3) 其他类型 21(31.3) 10(52.6) ECOG 评分(例,%) χ2=2.054 0.152 <2分 41(61.2) 15(78.9) ≥2分 26(38.8) 4(21.1) aaIPI评分(例,%) χ2=0.367 0.545 <2分 30(44.8) 10(52.6) ≥2分 37(55.2) 9(47.4) 移植前化疗方案数(例,%) χ2=11.949 <0.001 <2 44(65.7) 4(21.1) ≥2 23(34.3) 15(78.9) 移植时机(例,%) χ2=19.897 <0.001 挽救治疗组 11(16.4) 13(68.4) 一线巩固治疗组 56(83.6) 6(31.6) 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;RECIL为淋巴瘤疗效评价标准;SUVmax为最大标准化摄取值;DLBCL为弥漫大B细胞淋巴瘤;NKTCL为自然杀伤/T细胞性淋巴瘤;ECOG为东部肿瘤协作组体能状态;aaIPI为以年龄调整的国际预后指数 表 2 行自体造血干细胞移植的非霍奇金淋巴瘤患者的临床特征、18F-FDG PET/CT参数、RECIL与3年总生存率关系的单因素Cox比例风险回归分析
Table 2. Univariate Cox proportional risk regression analysis of the relationship between clinical features, 18F-FDG PET/CT parameters, response evaluation criteria in lymphoma and 3-year overall survival rate in patients with non-Hodgkin's lymphoma undergoing autologous hematopoietic stem cell transplantation
因素 HR值 95%CI P值 性别 1.587 0.343~7.350 0.555 年龄 1.035 0.991~1.080 0.119 移植前SUVmax 0.896 0.466~1.722 0.741 移植后SUVmax 1.177 1.087~1.274 <0.001 Ann Arbor分期 0.227 0.029~1.775 0.158 组织病理学类型 1.544 0.764~3.121 0.226 结外受累数目 1.158 0.339~3.962 0.815 ECOG 评分 5.932 0.759~46.377 0.090 aaIPI 评分 1.969 0.576~6.731 0.280 RECIL 0.020 0.003~0.155 <0.001 移植前化疗方案数 6.197 1.338~28.711 0.020 移植时机 8.808 2.289~33.891 0.002 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;RECIL为淋巴瘤疗效评价标准;SUVmax为最大标准化摄取值;ECOG为东部肿瘤协作组体能状态;aaIPI为以年龄调整的国际预后指数;HR为风险比;CI为置信区间 表 3 行自体造血干细胞移植的非霍奇金淋巴瘤患者的临床特征、18F-FDG PET/CT参数、RECIL与3年总生存率关系的多因素Cox比例风险回归分析
Table 3. Multivariate Cox proportional risk regression analysis of the relationship between clinical features, 18F-FDG PET/CT parameters, response evaluation criteria in lymphoma and 3-year overall survival rate in patients with non-Hodgkin's lymphoma undergoing autologous hematopoietic stem cell transplantation
因素 HR值 95%CI P值 RECIL 0.040 0.004~0.439 0.008 移植后SUVmax 1.039 0.877~1.229 0.660 移植前化疗方案数 2.108 0.307~14.477 0.448 移植时机 1.756 0.382~8.081 0.469 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;RECIL为淋巴瘤疗效评价标准;SUVmax为最大标准化摄取值;HR为风险比;CI为置信区间 -
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