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Journal of Clinical Oncology, Vol 25, No 34 (December 1), 2007: pp. 5435-5441 © 2007 American Society of Clinical Oncology. DOI: 10.1200/JCO.2007.12.2473 Positron Emission Tomography for Staging of Pediatric Sarcoma Patients: Results of a Prospective Multicenter Trial
From the Klinik für Pädiatrie m.S. Onkologie und Hämatologie; Otto-Heubner-Zentrum and Klinik für Strahlenheilkunde, Bereiche Nuklearmedizin und Radiologie inklusive Abteilung für Kinderradiologie; Campus Virchow-Klinikum, Charité–Universitätsmedizin Berlin, Berlin; and Klinik für Kinder Onkologie, Hämatologie, und Immunologie and Nuklearmedizinische Klinik, Universitätsklinikum Düsseldorf, Heinrich Heine Universität Düsseldorf, Düsseldorf, Germany Address reprint requests to Timm Denecke, MD, Klinik für Strahlenheilkunde, Bereiche Nuklearmedizin und Radiologie, Campus Virchow-Klinikum, Charité–Universitätsmedizin Berlin, Augustenburger Platz 1, D-13353 Berlin, Germany; e-mail: timm.denecke{at}charite.de
Purpose The objective of this study was to evaluate the impact of positron emission tomography (PET) using fluorine-18–fluorodeoxyglucose (FDG) for initial staging and therapy planning in pediatric sarcoma patients. Patients and Methods In this prospective multicenter study, 46 pediatric patients (females, n = 22; males, n = 24; age range, 1 to 18 years) with histologically proven sarcoma (Ewing sarcoma family tumors, n = 23; osteosarcoma, n = 11; rhabdomyosarcoma, n = 12) were examined with conventional imaging modalities (CIMs), including ultrasound, computed tomography (CT), magnetic resonance imaging, and bone scintigraphy according to the standardized algorithms of the international therapy optimization trials, and whole-body FDG-PET. A lesion- and patient-based analysis of PET alone and CIMs alone and a side-by-side (SBS) analysis of FDG-PET and CIMs were performed. The standard of reference consisted of all imaging material, follow-up data (mean follow-up time, 24 ± 12 months), and histopathology and was determined by an interdisciplinary tumor board. Results FDG-PET and CIMs were equally effective in the detection of primary tumors (accuracy, 100%). PET was superior to CIMs concerning the correct detection of lymph node involvement (sensitivity, 95% v 25%, respectively) and bone manifestations (sensitivity, 90% v 57%, respectively), whereas CT was more reliable than FDG-PET in depicting lung metastases (sensitivity, 100% v 25%, respectively). The patient-based analysis revealed the best results for SBS, with 91% correct therapy decisions. This was significantly superior to CIMs (59%; P < .001). Conclusion In staging pediatric sarcoma, subsidiary FDG-PET scanning depicts important additional information and has a relevant impact on therapy planning when analyzed side-by-side with CIMs.
Most pediatric sarcoma patients in Germany are enlisted in international trials, such as the Cooperative Osteosarcoma Study (COSS96) or, alternatively, the European and American Osteosarcoma Study Group trial (EURAMOS01), the European Ewing Tumor Working Initiative of National Groups trial (EURO-E.W.I.N.G.99), or the cooperative soft tissue sarcoma study (Cooperative Weichteilsarkom-Studie CWS-2002P). Within these trials on Ewing sarcoma family tumors (EWS), osteosarcoma (OS), and rhabdomyosarcoma (RMS), the overall 5-year survival rates were successfully increased by up to 60%.1-7 These trials on different tumor entities have a similar therapeutic concept in common, which is the combination of systemic multiagent chemotherapy and local treatment comprising surgery and/or irradiation to the primary tumor and all metastatic sites accessible.1-12 Lesions not (sufficiently) treated locally are associated with poor outcome and local treatment failure.13-17 Thus, diagnostic imaging has a strong impact on the course of chemotherapy by contribution to risk branch determination and the visualization of target lesions for local therapy. The staging algorithms of the aforementioned trials include a broad spectrum of diagnostic modalities. However, there are shortcomings of these standardized algorithms because metastases may lie outside the field of view of the employed imaging tools and the sensitivity for detecting bone or lymph node involvement is known to be limited.18-21 Metabolic whole-body imaging with positron emission tomography (PET) using fluorine-18–fluorodeoxyglucose (FDG) as tracer (FDG-PET) is a promising approach to compensate for these shortcomings. In adult sarcoma patients, however, it was shown that FDG-PET without computed tomography (CT) and magnetic resonance imaging (MRI) is not sufficient for appropriate pretherapeutic staging; it has been described as advantageous when used in addition to CT and MRI.22-24 The limited data available on the use of FDG-PET in pediatric sarcoma patients are promising but not sufficient to definitely conclude on the value of this method.20,21,25-27 To contribute to the determination of the diagnostic value of FDG-PET in pediatric oncology, we initiated a prospective multicenter trial in sarcomas of childhood and adolescence. The aim of the present analysis was to evaluate FDG-PET alone and as a supplement compared with the standard imaging procedures for initial staging and therapy planning in pediatric patients with EWS, OS, and RMS.
Patients Between December 2003 and October 2006, 46 pediatric patients (females, n = 22; males, n = 24; age range, 1 to 18 years; mean age, 12.9 ± 4.2 years) with histologically proven sarcomas (EWS, n = 23; OS, n = 11; and RMS, n = 12) from four institutions were enrolled onto this prospective multicenter study (Appendix Table A1, online only). Nine patients died during follow-up. Follow-up periods for the remaining patients ranged from 4 to 44 months (mean, 24 ± 12 months). Exclusion criteria were a life-threatening impairment of organ function, pregnancy, diabetes mellitus, and age less than 1 or more than 18 years. A written informed consent was obtained from all patients or parents. The study was in accordance with the Declaration of Helsinki and the principles of good clinical practice. The study protocol was approved by the local ethics committee. Furthermore, approval was granted by the German Federal Office on Radiation Protection (Bundesamt für Strahlenschutz) as well as the corresponding local authorities. Initial staging with conventional imaging modalities (CIMs) and the following therapy were performed according to the protocols of the national and international therapy optimization trials (ie, COSS96, EURAMOS01, EURO-E.W.I.N.G.99, and CWS-2002P). In addition to the standard procedures, patients were examined with whole-body FDG-PET.
CIMs CIMs were digitally imported to a work station (AdvantageWindows 4.1; GE Medical Systems, Milwaukee, IL) and reviewed by two radiologists in consensus, who were blinded to the results of FDG-PET and clinical follow-up data. Bone scintigraphy, read by a nuclear medicine physician, was analyzed side-by-side with the other CIMs. A therapy decision according to the protocols of the international therapy optimization trials was determined based on the histologic entities and pattern of tumor spread.
FDG-PET
Verification of Findings
Statistics
Primary Tumors All primary tumors were histologically proven before inclusion. In three patients (all RMS), the primary tumor was partially resected at external institutions for tumor reduction (n = 2) and/or to obtain material for histopathologic evaluation (n = 2). Of the remaining 43 tumors, biopsies were taken. FDG-PET and CIMs were equally effective in the detection of the primary tumors, and all 43 primary tumors and the three residual primary tumors were correctly identified by both methods (accuracy, 100%). The mean initial SUV of all primary sarcomas was 9.6 ± 4.8. Remarkably, OS showed a significantly higher SUV (13.3 ± 5.5) compared with the subgroups with EWS (9.0 ± 3.9; P = .030) and RMS (7.0 ± 3.4; P = .001). There was no significant difference in SUV between EWS and RMS (P = .110).
Lymph Node Metastases
Four of 46 patients had RMS of the extremities and, therefore, underwent regional lymph node sampling. In one of these patients, CIMs, PET, and biopsy were concordantly negative for the sampling region. In one patient, a sampled lymph node metastasis was false negative with CIMs and true positive with PET (Fig 1), whereas CIMs, PET, and histology were concordantly positive in the remaining two patients.
Bone Metastases The group of patients who received bone scintigraphy (total, n = 33; EWS, n = 17; OS, n = 12; RMS, n = 4) showed osseous tumor spread with a total number of 80 lesions (EWS, n = 49; OS, n = 31; histologically proven lesions including two false positives, n = 10). This affected 10 of 33 patients (EWS, n = 6; OS, n = 4). FDG-PET detected 71 of 80 lesions and reached a sensitivity of 89%, whereas CIMs including bone scintigraphy revealed a sensitivity of 57% (Table 1). CIMs (including bone scintigraphy) showed a higher number of false-negative lesions (n = 34) compared with FDG-PET. Three of these CIM-negative lesions were metastases from OS, and 31 occurred in EWS patients (Fig 2). Thus, the lesion-based sensitivities of FDG-PET and CIMs for detection of skeletal metastases were equal in patients with OS (FDG-PET, 90%; CIMs including bone scan, 90%; bone scan alone, 81%) and significantly different in patients with EWS (FDG-PET, 88%; CIMs including bone san, 37%; P < .01).
In the patient-based analysis of the group examined with bone scan, FDG-PET correctly identified all 10 patients with bone involvement, whereas CIMs showed false-negative results in three patients with EWS (Table 2). Stratifying for tumor entities, the sensitivity of SBS was 92% in EWS lesions and 100% for OS metastases. In the examination-based analysis, SBS analysis did not change the data derived from FDG-PET alone (Table 2).
Lung Metastases The patient-based analysis regarding the pulmonary staging consequently showed superior results of CIMs, with a sensitivity of 100% (nine of nine patients), whereas the sensitivity of FDG-PET was 56% (five of nine patients). FDG-PET failed to detect lung involvement in two patients with EWS, one patient with OS, and one patient with RMS (Table 2).
Therapy Modification
In OS patients, risk grouping is dependent on the response to neoadjuvant therapy rather than initial staging. Therefore, risk branch alterations could only be made in EWS and RMS patients. None of four RMS patients and four (24%) of 17 EWS patients (three with intensification of systemic therapy and one who was assigned to a lower risk branch) had risk branch alterations (Table 3). Concerning local therapy, there were eight patients (EWS, n = 6; RMS, n = 2) with expansion of the radiation field as a result of additional lesions, whereas, in one patient (EWS), the radiation field was reduced because CIMs showed false-positive bone lesions. In the remaining patient (OS), additional surgery was indicated (Table 3). The definition of the entire treatment plan for each patient including all target lesions for local therapy and the risk branch assignment for systemic treatment was correct in 67% of cases (22 of 33 patients) when derived from CIMs alone. The proportion of correct therapy plans based on PET alone (76%; 25 of 33 patients) was higher compared with CIMs alone but did not reach the level of significance (P = .505). A further improvement of accurate therapy planning was possible with correlative image analysis with PET and CIMs (SBS), with correct therapy assignment in 91% of patients (30 of 33 patients), which was significant compared with CIMs alone (P < .013; Table 4). The three patients with incorrect plans according to SBS analysis included one patient with concordantly false-positive bone lesions in CIMs and PET. In the remaining two patients, the expansion of local therapy based on SBS analysis was correct; however, visualization of CIMs-negative lesions in FDG-PET was incomplete for both patients.
In this prospective study enrolling 46 pediatric and adolescent patients, FDG-PET was performed for pretherapeutic staging of bone sarcomas and RMS. When assessing the primary tumor with FDG-PET in adult sarcoma patients, it has been shown that the metabolic activity as measured by FDG-PET before therapy correlates with the grade of tumor differentiation and prognosis.22,24 For the pediatric patient population, a study with 29 patients showed a significantly prolonged event-free and overall survival for OS with low FDG uptake at baseline.30 In EWS, however, SUV at baseline does not seem to be a prognostic factor.31 In the present study, the follow-up periods are too short to reliably assess a relationship of initial FDG uptake and survival. Interestingly, SUV was significantly higher in OS compared with EWS and RMS. This feature might add to the characterization of pediatric primary bone tumors in the future. Radiography and MRI certainly remain the most important imaging modalities for assessment of the primary tumor and the present study mainly focused on the value of FDG-PET for whole-body staging. The results of the present study indicate a high additional value of whole-body FDG-PET scanning regarding the detection of additional lesions compared with the standard diagnostic procedures. This advantage was partly a result of a methodic shortcoming of the standard diagnostic algorithm consisting of MRI, CT, and US. Metastatic deposits are not necessarily located within the field of view of these imaging methods and may be missed if not detectable on physical examination. Furthermore, the accuracy for detecting tumor deposits in the different tissues (bone or lymph nodes) is variable.18-21 In the subgroup of patients who received bone scintigraphy, FDG-PET was clearly superior in detecting bone lesions (sensitivity, 89% v 57% for CIMs). The superiority of FDG-PET was most prominent in the subgroup of EWS patients (sensitivity, 88% v 37% for CIMs). In OS patients, the sensitivities of FDG-PET (90%) and bone scan (81%) were not significantly different. These findings are similar to those of a retrospective study that revealed a higher sensitivity for FDG-PET (88%) compared with bone scan (69%) regarding the detection of bone metastases in 38 EWS patients, whereas bone scintigraphy was superior to FDG-PET in 32 OS patients.20 A possible explanation for the high scintigraphic detection rate of skeletal OS metastases is the production of osteoid and osteoblastic activity.20,32 EWS, however, tends to infiltrate the bone marrow rather than the mineralized bone, and osteodestruction is dominated by osteoclastic activity.20,33 The superiority of FDG-PET in pediatric EWS is strengthened by a report on 23 patients, in which PET depicted 67 of 68 bone metastases, whereas bone scintigraphy visualized only eight lesions.21 On the basis of these data and the results of the present study, bone scintigraphy seems to be replaceable in staging EWS. Regional lymph node involvement in RMS has been described to be a strong prognostic factor, which is why regional sampling of primary tumors in the extremities or paratesticular region has been recommended.34 In our series, there were four RMS patients with RMS of the extremities. FDG-PET was capable of detecting lymph node involvement accurately in all sampling regions, whereas CIMs revealed one false-negative result. In the total RMS group of our series, FDG-PET revealed a high patient-based sensitivity of 88% regarding lymph node metastases. In a recently published retrospective analysis of 24 RMS patients, Klem et al26 reported a limited region-based sensitivity and a high specificity (95%) for FDG-PET in nodal staging. In view of these results, further studies should address the question of whether clearly positive FDG-PET findings could obviate the need for routine sampling. Regarding the detection of small pulmonary metastases in FDG-PET, blurring caused by breathing motion and partial volume effect is known to cause false-negative results, resulting in a clear superiority of chest CT for the detection of pulmonary metastases from primary bone tumors.25 In the present study, a low sensitivity of FDG-PET (25%) was observed for pulmonary metastases, which was strongly dependent on lesion size because all false-negative lesions were smaller than 7 mm. These results show that chest CT is indispensable in staging pediatric sarcoma. Considering the results presented herein, the complementary character of CIMs and FDG-PET is obvious. SBS analysis revealed the highest proportion of correct therapy plans (91%), and its superiority to the standard algorithm using CIMs (67%) was significant. Correct therapy alterations as a result of FDG-PET were predominantly present in EWS (41%) and RMS patients (50%), whereas FDG-PET had less impact on the therapy management in OS patients (8%). A majority of these changes (30% of all patients) regarded local therapy application to metastatic sites. However, a relevant proportion of EWS patients (24%), switched their risk branch as well. The high rate of therapy optimizations in EWS patients is mainly a result of the superiority of FDG-PET in the detection of bone lesions, which was also reported by two other studies.20,21 In RMS, lymph node staging by FDG-PET is valuable and was responsible for the majority of therapy alterations in this subgroup. In OS patients, however, there is only little impact of FDG-PET on therapy planning because bone scan seems to be equally suited to detect skeletal involvement and chest CT is the method of choice for pulmonary staging.20,25 In summary, FDG-PET in SBS analysis with CIMs is a valuable tool for precise initial staging of pediatric sarcoma patients, has relevant impact on therapy decisions, and may contribute to further improve their outcome. SBS analysis of FDG-PET and CIMs should be performed in a prospective manner in large-scale trials of pediatric patients suffering from EWS, OS, and RMS to determine the prognostic value of staging by SBS compared with the prognostic value of staging by CIMs alone.
The author(s) indicated no potential conflicts of interest.
Conception and design: Günter Henze, Holger Amthauer Administrative support: Timm Denecke, Günter Henze, Holger Amthauer Provision of study materials or patients: Thomas Völker, Timm Denecke, Stefan Schönberger, Michail Plotkin, Juri Ruf, Brigitte Stöver, Hubertus Hautzel, Günter Henze, Holger Amthauer Collection and assembly of data: Thomas Völker, Timm Denecke, Ingo Steffen, Daniel Misch, Stefan Schönberger, Michail Plotkin, Juri Ruf, Christian Furth, Brigitte Stöver, Hubertus Hautzel, Günter Henze, Holger Amthauer Data analysis and interpretation: Thomas Völker, Timm Denecke, Ingo Steffen, Daniel Misch, Michail Plotkin, Juri Ruf, Brigitte Stöver, Günter Henze, Holger Amthauer Manuscript writing: Timm Denecke, Daniel Misch, Günter Henze Final approval of manuscript: Thomas Völker, Timm Denecke, Ingo Steffen, Daniel Misch, Stefan Schönberger, Michail Plotkin, Juri Ruf, Christian Furth, Brigitte Stöver, Hubertus Hautzel, Günter Henze, Holger Amthauer
We gratefully acknowledge the contribution of all physicians and associates of the participating institutes: the Departments for Pediatric Oncology and Nuclear Medicine of the Helios Klinikum Berlin-Buch, the Universitätsklinikum Leipzig, the Universitätsklinikum Düsseldorf, and the Charité–Universitätsmedizin Berlin.
Supported by Grant No. 50-2714-He 1 from the Deutsche Krebshilfe e.V. T.V. and T.D. contributed equally to this work. Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Semin Pediatr Surg 15:57-62, 2006[CrossRef][Medline] Submitted April 19, 2007; accepted September 6, 2007.
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Copyright © 2007 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
