Abstract
Investigators from the International Society of Paediatric Oncology Renal Tumour Study Group (SIOP-RTSG) report on outcomes of children with bilateral Wilms tumour treated on the SIOP 2001 study. They demonstrate that vincristine and actinomycin-D induction chemotherapy is sufficient in a subset of children, but most required additional agents during their treatment.
In both Europe and North America, neoadjuvant chemotherapy and bilateral nephron-sparing surgery are employed in the treatment of bilateral Wilms tumour (BWT) to preserve the greatest possible volume of functioning renal parenchyma [1]. Children with BWT are prone to develop diffuse anaplasia or to experience late disease relapse (>2 years) at higher rates than children with unilateral Wilms tumour [2]. These late relapses may be metachronous, “new” tumours due to germline or mosaic Wilms tumour genetic or epigenetic predisposition in patients with BWT [3, 4]. Furthermore, children with BWT experience higher rates of late renal failure resulting in the need for dialysis or kidney transplant when compared to patients with unilateral Wilms tumour [5]. Nevertheless, the imperative to preserve kidney function must be balanced against oncologically sound treatment aimed to eradicate tumour and optimise event-free and overall survival. Studies conducted primarily in Europe through the International Society of Paediatric Oncology Renal Tumour Study Group (SIOP-RTSG) and in North America through the Children’s Oncology Group (COG) have aimed to determine the optimal therapeutic approach, sequence, and intensity for patients with BWT.
In 2017, results were published from the COG Study AREN0534, which was the first prospective, multi-institutional clinical trial for children with BWT [6]. This study aimed to improve event-free and overall survival while maximising renal preservation in children with BWT by intensifying preoperative chemotherapy to include vincristine, actinomycin-D and doxorubicin (VAD), incorporating information from post-chemotherapy treatment histology to guide intensification of adjuvant chemotherapy when indicated, and emphasising renal preservation using bilateral nephron-sparing surgery whenever possible. In this study, surgery was to be performed no later than after 12 weeks of neoadjuvant chemotherapy. The COG AREN0534 study reported 4-year event-free survival (EFS) of 82.1% (95%CI: 73.5–90.8%) and overall survival of 94.9% (95% CI: 90.1–99.7%), which represented improvement when compared with BWT results from the previous National Wilms Tumour (NWTS-5) study (4-year EFS of 56%). On AREN0534, surgical approaches included unilateral total nephrectomy with contralateral nephron-sparing surgery 48% of the time and bilateral nephron-sparing surgery 35% of the time [6]. A recent follow-up report detailed the long-term oncologic outcomes of BWT patients treated on AREN0534, which included an 8-year event-free survival of 75% (69–83%), demonstrating the possibility of late relapse even beyond 4 years when compared to the 4-year EFS data [7].
In the current study conducted by the SIOP-RTSG, Sudour-Bonnange et al. [8] report the encouraging outcomes of children treated for BWT on the SIOP 2001 prospective international study protocol across 26 countries. They report a 5-year event-free survival of 76.1% and an overall survival of 88.1% in 174 patients treated for synchronous BWT on the study. The study also reports outcomes for 101 children with unilateral Wilms tumour with contralateral nephroblastomatosis and 52 children with bilateral nephroblastomatosis. The standardised approach to neoadjuvant chemotherapy in this study was two-drug therapy with four-week cycles of vincristine and actinomycin-D (VA), continued until surgery was deemed feasible. Continuation of 4-week cycles of VA or intensification of neoadjuvant chemotherapy to include doxorubicin was allowed at the discretion of a multidisciplinary treatment team until surgery was performed. Eighty-one patients with BWT in this study underwent surgery at <12 weeks, and 92 did at \(\ge\)12 weeks. Among the 174 BWT patients, 101 (59.7%) underwent unilateral total nephrectomy with contralateral nephron-sparing surgery, 48 (28.4%) underwent bilateral nephron-sparing surgery, and 20 (11.8%) underwent bilateral total nephrectomy.
In this study, adjuvant chemotherapy was intensified when indicated according to surgical staging and SIOP post-chemotherapy histology. In the entire study cohort of 327 children (which includes 101 children with unilateral WT and contralateral nephroblastomatosis and 52 children with bilateral nephroblastomatosis), two-drug VA chemotherapy was employed throughout treatment in 58.7% of patients and in 65.6% without metastatic disease. However, among the 174 patients with BWT, 50 (28.7%) exhibited poor volumetric tumour response to VA and subsequently received either neoadjuvant doxorubicin or another intensified chemotherapy agent in addition to VA. Regarding adjuvant chemotherapy administered to 156 of 174 evaluable patients with BWT treated on the study based on post-treatment histology, 55 (36%) received VA alone, 48 (30%) received VAD, 30 (19%) received four drugs including etoposide, carboplatin, cyclophosphamide, and doxorubicin, and 23 (15%) received other adjuvant chemotherapy treatment. In summary, a minimum of 64% of patients with BWT treated on this study required additional chemotherapy drugs beyond VA at some point during their therapy.
The current report demonstrates that VA alone is sufficient treatment in a subgroup of patients with BWT (particularly those who were ultimately deemed to have Stage I disease and had a 94.4% 5-year EFS), but also shows that most patients with BWT treated on the SIOP 2001 protocol required intensification of chemotherapy at some point in their treatment due to metastatic disease, poor volumetric response to induction therapy, or information from surgical staging and post-treatment histology. In the context of the previous COG AREN0534 study, it is probable that the North American VAD induction approach over-treats a subset of patients while the European/SIOP VA initial induction approach under-treats a subset of patients with BWT.
Future refinements in identifying which children with BWT require two-drug versus three-drug (or other) induction chemotherapy may be possible by maximising the information known about the tumours at diagnosis. Biopsy is not typically considered a feasible way to understand these scenarios because an innumerable number of biopsies may be required in BWT due to intertumoral genetic heterogeneity among bilateral and multifocal tumours and intratumoral genetic heterogeneity within each tumour [9]. Therefore, future alternative approaches might include the identification of clinically relevant copy number or genetic variants in circulating tumour DNA, radiomic evaluation based on CT or MRI characteristics, or more precise evaluation of germline genetic or epigenetic predisposition for BWT at diagnosis [10]. These possibilities are promising areas for future translational research.
Furthermore, both the COG AREN0534 and SIOP 2001 BWT studies demonstrate the future opportunity to increase the number of bilateral nephron-sparing surgeries performed for patients with BWT to preserve kidney function. Standardisation of surgical timing to avoid protracted chemotherapy, development of diffuse anaplasia, and late toxicity also remains imperative in future BWT treatment protocols.
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Murphy, A.J. Pursuit of the optimal therapeutic approach and intensity for children with bilateral Wilms tumour. Br J Cancer 131, 970–971 (2024). https://doi.org/10.1038/s41416-024-02806-4
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DOI: https://doi.org/10.1038/s41416-024-02806-4