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Other Comparisons of Autologous BMT and Chemotherapy—Previous smaller studies comparing autologous marrow transplantation to chemotherapy had yielded conflicting results, with Pinkerton reporting the only randomized trial showing a significant improvement with autologous BMT.[32] This report included a total of only 65 patients, however.
Overall, autologous BMT appears to be at least as effective as intensive chemotherapy and may provide an advantage in some extremely high-risk subgroups.
Another ongoing phase I dose-escalation study of a non-TBI-containing myeloablative regimen has thus far shown event-free survival comparable to that seen in the previous 321P3 study (55% at 2 years from autologous BMT). The most recently completed CCG trial in high-risk disease was designed to answer, in a prospective, randomized fashion, the relative importance of ablative therapy with purged autologous BMT vs intensive consolidation. The outcome of this study, still blinded for analysis, will help determine the future role of myeloablative therapy, as well as the potential utility of differentiating agents, in high-risk neuroblastoma. The source and purity of the stem cells used for ablative therapy in neuroblastoma have been the focus of concern. More recently, testing of peripheral blood stem-cell collections and bone marrow with PCR has confirmed the problem of contamination with tumor cells, even in CD34-selected preparations.
Dose-intensive therapy, with or without stem-cell support, is rapidly approaching the limits of toxicity, both in terms of acute and late effects. Phase I and II studies of anti-GD2 antibodies have shown some modest antitumor efficacy in patients with relapsed neuroblastoma.[38,39] Both the murine monoclonal 3F8 and 14G2a (murine), the latter tested with IL-2 and with GM-CSF, have shown some tumor responses, as well as in vitro stimulation of antibody-dependent cellular cytotoxicity (ADCC). Targeted therapy using antibody or MIBG for the delivery of radiation in the form of iodine-131 has also been tested in clinical trials. Iodine-131-MIBG has been widely tested in Europe for refractory neuroblastoma and, more recently, for initial therapy in patients with regional disease. Differentiating agents are another approach for circumventing the undesirable effects of cytotoxic agents.
Currently, various derivatives of retinoic acid are the differentiating compounds in clinical testing. Other retinoids currently in phase I investigation include all-trans-retinoic acid (ATRA [Vesanoid]) combined with interferon-alfa (Intron A, Roferon-A), 9-cis-retinoic acid, and fenretinide, another analog that causes growth arrest and apoptosis in vitro, even in cell lines shown to be resistant to trans-retinoic acid.
Substantial advances are occurring in the elucidation of the molecular pathogenesis of neuroblastoma, as well as in the definition of clinical prognostic groups. These patients continue to respond poorly even to very dose-intensive therapy, although incremental advances have certainly been made over the past decade. All three studies treated patients with five to six cycles of induction chemotherapy consisting of cisplatin (Platinol), doxorubicin, cyclophosphamide, and etoposide (VePesid). With a median follow-up of 5 years, the event-free survival at 5 years from the time of autologous BMT for 147 patients is 37%.
However, a definitive conclusion cannot be made until the results of a recently completed CCG randomized prospective trial comparing outcomes among unselected high-risk patients from the time of diagnosis become available. This phase I study has further verified the earlier suggestion from Kushner and co-workers[28] that higher-dose local irradiation to tumor sites may prevent primary site relapse, a common problem in previous CCG protocols.

Current and future studies will examine repetitive stem-cell transplants, more intensive induction therapies, and the use of alternative stem-cell sources. Immunocytology techniques have shown that as many as 70% of patients have bone marrow tumor at diagnosis and 50% have circulating tumor cells in peripheral blood. This has been inferred from studies showing the development of tumor cell lines from harvested bone marrow and by reports of miliary lung metastases following autologous BMT,[35] and has been demonstrated more definitively by the gene-marking studies of Rill and co-workers.[36] In these gene-marking studies, autologous unpurged but histologically tumor-free marrow was transfected with the neomycin resistance gene and then reinfused into patients, some of whom subsequently relapsed with neuroblastoma tumors expressing the marker. The significance of such low-level contamination is still undetermined but will be examined in future studies. Novel approaches that are more tumor-specific and less toxic are required to make further progress in metastatic neuroblastoma. Cheung and co-workers have documented responses to iodine-131-3F8 among patients with refractory neuroblastoma,[41] and are currently conducting a study in which newly diagnosed patients are receiving iodine-131-3F8 in ablative doses followed by bone marrow rescue, with further treatment with cold antibody post-transplant. We have conducted a phase I dose escalation trial of iodine-131-MIBG at the University of California (San Francisco) and have determined the maximal non-marrow-ablative dose and the maximal practical ablative dose with stem-cell rescue.[42] In 30 patients, we observed a 37% response rate and no significant toxicity other than hematologic effects. For many years, laboratory studies have shown the capacity for either spontaneous or induced differentiation and growth arrest of neuroblastoma cell lines in culture. In addition, modest but significant improvements in the treatment of metastatic disease have been achieved by increasing dose intensity with the use of hematopoietic support. Suzuki T, Yokota J, Mugishima H, et al: Frequent loss of heterozygosity on chromosome 14q in neuroblastoma. Plantaz D, Mohapatra G, Matthay KK, et al: Gain of the chromosome 17 is the most frequent abnormality detected in neuroblastoma by CGH. Seeger RC, Brodeur GM, Sather H, et al: Association of multiple copies of the N-myc oncogene with rapid progression of neuroblastomas.
Crabbe DCG, Peters J, Seeger RC: Rapid detection of MYCN gene amplification in neuroblastomas using the polymerase chain reaction. Suzuki T, Bogenmann E, Shimada H, et al: Lack of high affinity nerve growth factor receptors in aggressive neuroblastomas. Hiyama E, Hiyama K, Yokoyama T, et al: Correlating telomerase activity levels with human neuroblastoma outcomes. Shimada H, Stram DO, Chatten J, et al: Identification of subsets of neuroblastomas by combined histopathologic and N-myc analysis. Matthay KK, Sather HN, Seeger RC, et al: Excellent outcome of stage II neuroblastoma is independent of residual disease and radiation therapy.
Matthay K, Seeger R, Haase G, et al: Treatment and outcome for stage III neuroblastoma based on prospective biologic staging. Brodeur GM, Seeger RC, Barrett A, et al: International criteria for diagnosis, staging, and response to treatment in patients with neuroblastoma. Brodeur GM, Pritchard J, Berthold F, et al: Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment.

Moss TJ, Reynolds CP, Sather HN, et al: Prognostic value of immunocytologic detection of bone marrow metastases in neuroblastoma. Cheung NKV, Heller G: Chemotherapy dose intensity correlates strongly with response, median survival, and median progression-free survival in metastatic neuroblastoma.
Kushner BH, O’Reilly RJ, Mandell LR, et al: Myeloablative combination chemotherapy without total body irradiation for neuroblastoma. Matthay KK, Seeger RC, Reynolds CP, et al: Allogeneic vs autologous purged bone marrow transplantation for neuroblastoma.
Philip T, Zucker JM, Bernard JL, et al: Improved survival at 2 and 5 years in the LMCE1 unselected group of 72 children with stage IV neuroblastoma older than 1 year of age at diagnosis: Is cure possible in a small subgroup? Schuster JJ, Cantor AB, McWilliams N, et al: The prognostic significance of autologous bone marrow transplant in advanced neuroblastoma. Rill DR, Santana VM, Roberts M, et al: Direct demonstration that autologous bone marrow transplantation for solid tumors can return a multiplicity of tumorigenic cells. Reynolds CP, Seeger RC, Vo DD, et al: Model system for removing neuroblastoma cells from bone marrow using monoclonal antibodies and magnetic immunobeads. Matthay KK, Desantes K, Hasegawa B, et al: Phase I dose escalation of 131I-metaiodo-benzylguanidine (MIBG) with autologous bone marrow support in refractory neuroblastoma. Villablanca JG, Khan AA, Avramis VI, et al: Phase I trial of 13-cis-retinoic acid in children with neuroblastoma following bone marrow transplantation.
Reynolds CP, Kane DJ, Einhorn PA, et al: Response of neuroblastoma to retinoic acid in vitro and in vivo.
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After undergoing surgery for local control and receiving irradiation to residual disease sites, patients received ablative chemotherapy and total-body irradiation (TBI) with BMT or were continued on four-drug induction chemotherapy for a total of 13 cycles. By the end of five to seven courses of chemotherapy, 159 patients were event-free; 67 of these patients went on to receive autologous BMT, while 74 continued chemotherapy for a total of 1 year. However, the relapse rate for patients transplanted after first disease progression has continued to be high; the current event-free survival rate at 2 years post-transplantation is only 15%.
A second randomization, done at the end of chemotherapy consolidation or autologous BMT, assigned patients to receive or not to receive 6 months of 13-cis-retinoic acid (isotretinoin [Accutane]). The relative risk of an event after autologous BMT was only 58% of that with chemotherapy (P = .01).
In vitro and some in vivo studies have reported this differentiating agent to have efficacy against neuroblastoma.

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