Introduction: Poor survival of stage 4 neuroblastomas is largely due to a high relapse rate. We tested whether genomic analysis of disseminated tumor cells (DTCs) from the bone marrow helps to better understand the tumor evolution and to characterize the relapse-seeding clone.
Methods: Seven samples from different regions of the primary tumor, DTCs at diagnosis, metastatic tumor and DTCs at relapse were analyzed by SNP array in a stage 4 patient. Relapse-associated chromosomal aberrations found in this case were tested in a validation cohort of 122 DTC and 81 tumor samples from 154 stage 4 patients.
Results: In the case study, independent tumor evolution in the primary tumor and metastatic cells resulted in exclusive aberrations in each sample. DTCs at diagnosis, DTCs at relapse and the metastatic tumor displayed a unique aberration, i.e. 1q sub-terminal deletion, which was not found in any of the primary tumor samples. Thus, the relapse clone most likely originated from a clone presented in the DTCs at diagnosis.
In the validation cohort, 1q sub-terminal deletions/imbalances were found in 27.5% of the DTCs at relapse, 17.8% of the diagnostic DTCs and 11.1% of the primary tumors. Patients with 1q deletions/imbalances in the diagnostic DTCs had a higher chance of relapse or early death (5-years EFS: 18.8% vs 36%). Additionally, 19q deletion, significantly associated with 1q deletion/imbalance, was found in 27.5%, 15.1% and 12.3% of relapse DTCs, diagnostic DTCs and primary tumors, respectively. 19q deletion in the diagnostic DTCs was associated with decreased EFS (5-years EFS: 13.3% vs 42%) and OS (5-years EFS: 25.9% vs 38.9%).
Discussion: We provide evidence of branched clonal evolution and parallel progression of the primary tumor and metastatic cells. 1q sub-terminal deletions/imbalances were highly associated with relapse and were more frequently found in the DTCs at diagnosis compared to the primary tumors. Thus, analyzing DTCs at diagnosis may provide a higher probability for detecting the relapse founder clone compared to tumor biopsy.