van Zogchel Lieke M J, Decarolis Boris, van Wezel Esther M, Zappeij-Kannegieter Lily, Gelineau Nina U, Schumacher-Kuckelkorn Roswitha, Simon Thorsten, Berthold Frank, van Noesel Max M, Fiocco Marta, van der Schoot C Ellen, Hero Barbara, Stutterheim Janine, Tytgat Godelieve A M
Princess Máxima Center for Pediatric Oncology, Utrecht, The Netherlands.
Department of Experimental Immunohematology, Sanquin Research and Landsteiner Laboratory of the Amsterdam UMC, Amsterdam, The Netherlands.
J Exp Clin Cancer Res. 2024 Dec 26;43(1):331. doi: 10.1186/s13046-024-03261-y.
Liquid biopsies offer less burdensome sensitive disease monitoring. Bone marrow (BM) metastases, common in various cancers including neuroblastoma, is associated with poor outcomes. In pediatric high-risk neuroblastoma most patients initially respond to treatment, but in the majority the disease recurs with only 40% long-term survivors, stressing the need for more sensitive detection of disseminated disease during therapy.
To validate sensitive neuroblastoma mRNA RT-qPCR BM testing, we prospectively assessed serial BM samples from 345 international high-risk neuroblastoma patients, treated in trials NB2004 (GPOH) or NBL2009 (DCOG), using PHOX2B, TH, DDC, CHRNA3, and GAP43 RT-qPCR mRNA markers and BM GD2-immunocytology. Association between BM-infiltration levels and event-free survival (EFS) and overall survival (OS) was estimated by using Cox regression models and Kaplan-Meier's methodology.
BM infiltration >10% by RT-qPCR at diagnosis was prognostic for survival (adjusted hazard ratio (HR) 1.82 [95%CI 1.25-2.63] and 2.04 [1.33-3.14] for EFS and OS, respectively). Any post-induction RT-qPCR positivity correlated with poor EFS and OS, with a HR of 2.10 [1.27-3.49] and 1.76 [1.01-3.08] and 5-years EFS of 26.6% [standard error 5.2%] versus 60.4% [6.7] and OS of 43.8% [5.9] versus 65.7% [6.6] for RT-qPCR-positive patients versus RT-qPCR-negative patients. In contrast, post-induction immunocytology positivity was not associated with EFS or OS (HR 1.22 [0.68-2.19] and 1.26 [0.54-2.42]).
This study validates the association of not clearing of BM metastases by sensitive RT-qPCR detection with very poor outcome. We therefore propose implementation of RT-qPCR for minimal residual disease testing in neuroblastoma to guide therapy.
液体活检为疾病监测提供了负担较小的敏感方法。骨髓(BM)转移在包括神经母细胞瘤在内的多种癌症中很常见,与不良预后相关。在儿童高危神经母细胞瘤中,大多数患者最初对治疗有反应,但大多数患者疾病会复发,长期生存率仅为40%,这凸显了在治疗期间更敏感地检测播散性疾病的必要性。
为了验证敏感的神经母细胞瘤mRNA逆转录定量聚合酶链反应(RT-qPCR)骨髓检测方法,我们前瞻性地评估了345例国际高危神经母细胞瘤患者的系列骨髓样本,这些患者在NB2004(德国儿童肿瘤学组,GPOH)或NBL2009(荷兰儿童肿瘤学组,DCOG)试验中接受治疗,使用嗜铬粒蛋白2B(PHOX2B)、酪氨酸羟化酶(TH)、多巴脱羧酶(DDC)、胆碱能受体α3(CHRNA3)和生长相关蛋白43(GAP43)RT-qPCR mRNA标志物以及骨髓GD2免疫细胞学法。通过使用Cox回归模型和Kaplan-Meier方法估计骨髓浸润水平与无事件生存期(EFS)和总生存期(OS)之间的关联。
诊断时RT-qPCR检测骨髓浸润>10%对生存具有预后意义(EFS和OS的调整后风险比(HR)分别为1.82[95%置信区间(CI)1.25 - 2.63]和2.04[1.33 - 3.14])。诱导治疗后任何RT-qPCR阳性与不良的EFS和OS相关,RT-qPCR阳性患者与RT-qPCR阴性患者相比,HR分别为2.10[1.27 - 3.49]和1.76[1.01 - 3.08],5年EFS分别为26.6%[标准误5.2%]和60.4%[6.7%],OS分别为43.8%[5.9%]和65.7%[6.6%]。相比之下,诱导治疗后免疫细胞学法阳性与EFS或OS无关(HR分别为1.22[0.68 - 2.19]和1.26[0.54 - 2.42])。
本研究验证了通过敏感的RT-qPCR检测未清除骨髓转移与极差预后之间的关联。因此,我们建议在神经母细胞瘤中实施RT-qPCR用于微小残留病检测以指导治疗。