Keywords pediatric renal cell carcinoma, TFE3, Xp11.2 translocation carcinomas, prognosis

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1 Xp11.2 Translocation Renal Cell Carcinomas Have a Poorer Prognosis Than Non-Xp11.2 Translocation Carcinomas in Children and Young Adults: A Meta-analysis International Journal of Surgical Pathology 18(6) The Author(s) 2010 Reprints and permission: sagepub.com/journalspermissions.nav DOI: / Qiu Rao, MD 1, Bing Guan, MD 1, and Xiao-jun Zhou, MD, PhD 1 Abstract Objectives. Renal cell carcinomas (RCCs) in children and adolescents are much rarer than in adults. In this age group, Xp11.2 translocation RCCs were the most common subtype of pediatric RCCs. Information regarding the clinical behavior of pediatric RCCs remains controversial because of their relatively rare incidence. The authors aimed to perform a systematic review and meta-analysis to better define the biological features of pediatric RCCs. Methods. Eligible studies were identified through multiple search strategies. Studies were assessed for quality using the Jadad Quality Scale. Data were collected comparing overall survival (OS), disease-free survival (DFS), and stage in patients with TFE3 + pediatric RCCs and TFE3 RCCs. Results. A total of 4 studies were included for meta-analysis, and pooled odds ratios (ORs) with 95% confidence interval (CI) were calculated. The meta-analysis outcomes showed that TFE3 + pediatric RCCs were significantly associated with poorer outcomes (OS and DFS) and a higher stage (III/IV) than TFE3 RCCs (pooled ORs for each group: 4.59 [95% CI = ] for OS; 5.79 [95% CI = ] for DFS; and 5.89 [95% CI = ] for stage). This result was also confirmed by OS and DFS curves (P =.005 and P =.001). Conclusions. Xp11.2 translocation carcinomas appear to have a poorer prognosis than non-xp11.2 translocation carcinomas in children and young adults. Keywords pediatric renal cell carcinoma, TFE3, Xp11.2 translocation carcinomas, prognosis Introduction Pediatric RCCs are relatively rare and account for only 2% to 6% of all renal neoplasms in children and young adults. 1 Recent data suggest that pediatric RCCs may be a different entity from adult RCCs, with distinct morphological features and genetic abnormalities, and Xp11.2 translocation carcinomas are the most common subtype of pediatric RCCs. 2-4 In the 2004 WHO renal tumor classification, Xp11.2 translocation carcinomas have been recognized as a distinctive pathological entity from adult RCCs. 5 These translocation RCCs are characterized by a number of different translocations involving the Xp11.2 chromosome, all of which result in gene fusions involving the TFE3 gene. 6 At least 5 distinct gene fusions involving TFE3 have been characterized in the literature. 2,7 TFE3 protein is thought to be constitutively overexpressed in Xp11.2 translocation carcinomas and can be specifically identified by immunohistochemistry. 8,9 A recently developed antibody of TFE3 protein has been shown to be a highly sensitive (97.5%) and specific (99.6%) marker in these tumors. 8 Although pediatric RCCs were recognized as a new entity from adult RCCs, information regarding the clinical behavior of pediatric RCCs remains controversial because of their relatively rare incidence, as can be seen when reviewing published data with prognostic reports. Some studies have suggested a good outcome for pediatric RCCs despite lymph node metastases. 10,11 However, some cases of translocation carcinomas were previously reported to have an aggressive clinical course. 12,13 To better define the biological features of pediatric RCCs and determine whether clinical outcome of TFE3 + pediatric RCCs differed from TFE3 RCCs in 1 Department of Pathology, Clinical School of Medical College of Nanjing University/Nanjing Jinling Hospital, Nanjing, Jiangsu , China Corresponding Author: Xiao-jun Zhou, Department of Pathology, Clinical School of Medical College of Nanjing University/Nanjing Jinling Hospital, Nanjing, Jiangsu , China

2 Rao et al. 459 this age group, we performed a systematic review and meta-analysis. Materials and Methods Literature Search A computer-aided literature search of PubMed (MEDLINE), MEDLINE in-process and nonindexed citations, EMBASE, DARE, the Cochrane Library, Science Citation Index, and meeting abstracts was conducted. An initial search strategy using recognized search terms TFE3, prognosis, Xp11.2 translocation, and pediatric renal cell carcinomas was performed in July 2009 and then repeated in December Reference lists from identified primary studies were then searched to identify any studies missed by the electronic search strategies. Study Selection Abstracts of all candidate articles were read by 2 independent reviewers (QR and BG). Articles that could not be categorized based on title and abstract alone were retrieved for full-text review. These articles were independently read and checked for inclusion criteria. Disagreements were resolved through consensus with a third reviewer (XZ). Primary studies that reported data required for meta-analysis were identified and included. Authors of included studies were not contacted for additional, unreported data. Study Inclusion/Exclusion Criteria Inclusion criteria for primary studies were as follows: (1) All studies included TFE3 + pediatric RCCs and TFE3 pediatric RCCs with follow-up information; (2) all cases were submitted to immunostaining with TFE3 (SC-5958, Santa Cruz Biotechnology Inc, Santa Cruz, CA), and Xp11.2 translocation carcinomas were confirmed by TFE3 and/or molecular analysis. There was no language restriction for searching. Inclusion of otherwise eligible studies depended on the availability of translation resources for the language(s) concerned, but no such studies were identified. Reviews, nonoriginal articles, and case reports were excluded. All studies were carefully evaluated to identify duplicate patient populations. Criteria used to determine duplicate populations included study period, hospital, treatment information, and any additional inclusion criteria. Quality Assessment of Primary Studies Quality assessment was performed in each of the acceptable studies in duplicate by independent reviewers (QR and BG) using the Jadad Quality Scale. 14,15 Issues such as randomization, concealment of allocation, and blinding were assessed. Studies with a score 3 were considered to be of high quality. Data Extraction Data from all primary studies included were independently extracted by 2 reviewers (QR and BG). Data extraction fields for each study included the following: (1) demographic data regarding inclusion criteria, patient age, gender, and treatment during follow-up; (2) tumor data, including size, stage, grade, and metastases; (3) survival data, including overall survival (OS) and disease-free survival (DFS); and (4) other variables included number of patients lost and reasons for patients lost during follow-up. Our primary interest was to gather data on OS and DFS. We did, however, also perform analyses on stage because this was commonly reported in these studies. Data Analysis/Synthesis The studies included were divided into 3 groups for analysis: those with data regarding OS, those about DFS, and those regarding stage. Dichotomous data were expressed as odds ratios (ORs). Pooled ORs with 95% confidence intervals (CIs) were used in the Mantel-Haenszel fixed-effect model when no statistically significant heterogeneity was detected. A P of <.05 was chosen for significance. The heterogeneity of combined ORs was investigated using a χ 2 -based test of homogeneity and evaluation of the inconsistency index (I 2 ) statistic, which takes values from 0% to 100%. 16 We judged that heterogeneity was significant when the p value was less than 0.1. An I 2 value >50% was considered to represent substantial heterogeneity between studies. 17 In cases with substantial heterogeneity, random-effects models of DerSimonian-Laird were applied. Assessment of publication bias was performed for each of the pooled study groups using a funnel plot. All analyses were carried out using the statistical software Review Manager (Version 5.0 for Windows; the Cochrane Collaboration, Oxford, UK). We also estimated the OS and DFS curves between TFE3 + pediatric RCCs and TFE3 RCCs. Survival curves were constructed according to the method of Kaplan-Meier. Differences between the curves were assessed using the log rank test. A P of <.05 was considered statistically significant. Statistical analyses were performed using SPSS software, version 16.0 (SPSS, Chicago, IL). Results Description of Studies The abstracts and titles of 128 primary studies were identified for initial review using search strategies as described. Reviewers identified 118 potential studies for full-text

3 460 International Journal of Surgical Pathology 18(6) 118 studies identified using described search strategies 42 candidate studies 4 studies available for meta-analysis Figure 1. Flow chart of the meta-analysis Abbreviation: RCC, renal cell carcinoma. 76 excluded for case report and review 28 eliminated for inadequate data 10 excluded for only including TFE3 + pediatric RCCs review. On further review, 76 articles were eliminated because they were reviews or case reports; 28 were eliminated because there were inadequate data for meta-analysis, and 10 were excluded for only including TFE3 + pediatric RCCs (Figure 1). Given that several authors have multiple publications in this field, we took great care to ensure that data reported in each article were unique. Quality assessment using the Jadad Quality Scale, a composite scoring system with a maximum of 5 points, was performed on all 4 studies included for meta-analysis. 11,18-20 The following parameters were evaluated: randomized study, description of randomization, double-blinded study, description of double blinding, description of withdrawals, and dropouts. Studies with a total score greater than or equal to 3 were considered to be of high quality, whereas low-quality studies had scores less than or equal to 2. 14,21 The characteristics of retained studies are listed in Table 1. Publication bias is described as visual assessment of a funnel plot in Figure 2. There was no evidence for significant publication bias in each of the 3 pooled groups. Primary Outcomes In total, there were 83 patients in all 4 studies. The mean sample size for all studies was 20.8 patients (range, 11-46). The average age of all patients in 4 studies was 14.7 years (range, 2-25 years). Follow-up information and tumor stage were recorded for each of the included studies. Follow-up information was available for 76 cases, including 35 Xp11.2 translocation RCCs and 41 non-xp11.2 translocation carcinomas. Nephrectomy was performed at diagnosis in 70 patients; 12 patients underwent partial nephrectomy, and 1 patient underwent simple nephrectomy. The mean and median follow-up time was 60.9 and 50 months, respectively (range, months). Among the 35 patients with Xp11.2 translocation RCCs, 19 were alive with no evidence of disease, 14 died of disease, and 2 remained alive with disease. Of the 41 non-xp11.2 translocation carcinomas, 35 were alive and disease free at their most recent follow-up visits, 4 died of disease, and in 2 cases deaths were a result of other causes. Results of meta-analysis for OS and DFS showed that TFE3 + pediatric RCCs were significantly associated with a poorer OS and DFS than TFE3 RCCs with pooled ORs of 4.59 (95% CI = ) and 5.79 (95% CI = ), respectively (Figures 3A and 3B). There was no evidence for heterogeneity of the 4 available studies (I 2 statistic = 0%, P =.84; and I 2 statistic = 0%, P =.81). The pooled OR estimate for stage of the 4 studies was 5.89 (95% CI = ), with no evidence for significant heterogeneity between studies (I 2 statistic = 0%, P =.53). TFE3 + pediatric RCCs were significantly associated with a higher stage (III/IV) than TFE3 RCCs (Figure 3C). Survival Analyses Studying OS and DFS curves, we observed that TFE3 + pediatric RCCs were significantly more frequently associated with a poorer outcome than TFE3 RCCs (P =.005 and P =.001; Figure 4). Discussion RCCs in children and adolescents are much rarer than in adults. 22 In this age group, Xp11.2 translocation RCCs were the most common subtype of pediatric RCCs and have been recognized as a new entity in the 2004 WHO renal tumor classification. 1 The biological behavior of pediatric RCCs is controversial. Some studies have suggested a good prognosis for pediatric RCCs. 10,11 However, some cases of translocation carcinomas have been reported to have an aggressive clinical course. 12,13 In the study by Rais-Bahrami et al, 23 the authors suggested that Xp11.2 translocation RCCs have the potential for late recurrences. Geller et al 11 also reported that Xp11.2 translocation RCCs intended to present at advanced stage. When reviewing published articles with prognostic reports, there were few series of pediatric RCCs because of their relatively rare incidence, and a relevant systematic review with meta-analysis was lacking. In this study, we evaluated 4 primary studies from the published literature and compared OS, DFS, and stage in patients with TFE3 + pediatric RCCs and TFE3 RCCs. 11,18-20 Our metaanalysis outcomes showed that TFE3 + pediatric RCCs were significantly associated with poorer outcomes (OS and DFS) and a higher stage (III/IV) than TFE3 RCCs (pooled ORs for each group: 4.59 [95% CI = ] for OS; 5.79 [95% CI = ] for DFS; and 5.89 [95% CI = ] for stage). This result was also confirmed by OS and DFS curves (P =.005 and P =.001). Although we did not observe significant heterogeneity or publication bias between studies, it is important to note

4 Rao et al. 461 Table 1. Characteristics of Included Studies References Study Design Number of Patients (M/F) Number of Patients TFE3+/ TFE3 TFE3 Detection Method Geller et al 11 C, R 11 (3/8) 7/4 Antibody Ramphal et al 16 C, R 13 (5/8) 7/6 Antibody Rao et al 18 C, R 46 (17/19) 19/27 Antibody Wu et al 17 C, R 13 (9/4) 6/7 Antibody Treatment RN PN SN Tumor Stage I/II (III/IV) Odds Ratios Jadad Score (7) Estimated (5) Estimated (24) Estimated (4) Estimated 3 Abbreviations: C, consecutive; R, retrospective; RN, radical nephrectomy; PN, partial nephrectomy; SN, simple nephrectomy. Figure 2. Bias assessment plots for studies included in all 3 meta-analyses: there was no evidence for significant publication bias in any of the 3 pooled groups. Plots are arranged as follows: A. Overall survival. B. Disease-free survival. C. Stage evaluation Abbreviation: SE, standard error; OR, odds ratio; RCC, renal cell carcinoma.

5 462 International Journal of Surgical Pathology 18(6) Figure 3. Forrest plots and meta-analysis of studies evaluating odds ratios of TFE + pediatric RCCs as compared with TFE RCCs: survival and stage data are reported as follows: A. Overall survival. B. Disease-free survival. C. Stage evaluation Abbreviation: RCC, renal cell carcinoma; CI, confidence interval. Figure 4. Overall survival (A) and disease-free survival (B) analyses were computed comparing TFE + pediatric RCCs with TFE RCCs. TFE + pediatric RCCs were significantly more frequently associated with a poorer outcome than TFE RCCs (Kaplan-Meier analysis; P =.005 and P =.001) Abbreviation: RCC, renal cell carcinoma.

6 Rao et al. 463 that because of the small number and sample size of primary studies analyzed in each group, not extending our search criteria to other sources of unpublished data, with a number of patients in 1 study without follow-up, possibly leading to an attrition bias, could have potentially limited the power to detect important differences. The presented ORs might, therefore, be an overestimation of the true effect size. In conclusion, this meta-analysis of the current bestavailable evidence demonstrated that TFE3 + pediatric RCCs were significantly associated with a poorer outcomes (OS and DFS) and a higher stage (III/IV) than TFE3 RCCs. The results provide strong grounds for stating that any RCC in children and young adults should be subjected to immunostaining with TFE3, a highly sensitive (97.5%) and specific (99.6%) marker, 8 to identify these translocation carcinomas, and patients with TFE3 + pediatric RCCs could benefit from a stricter follow-up. We also recognize that this evidence must be interpreted with some caution because of the relatively poor quality of study design. Therefore, further investigations on larger and more heterogeneous studies should be carried out to validate and extend our results. Acknowledgment We are indebted to the authors of the primary studies included in this meta-analysis. Declaration of Conflicting Interests The author(s) declared no potential conflicts of interest with respect to the authorship and/or publication of this article. Funding The author(s) received no financial support for the research and/ or authorship of this article. References 1. Cook A, Lorenzo AJ, Salle JL, et al. Pediatric renal cell carcinoma: single institution 25-year case series and initial experience with partial nephrectomy. J Urol. 2006;175: ; discussion Argani P. The evolving story of renal translocation carcinomas. Am J Clin Pathol. 2006;126: Winarti NW, Argani P, De Marzo AM, et al. Pediatric renal cell carcinoma associated with Xp11.2 translocation/tfe3 gene fusion. Int J Surg Pathol. 2008;16: Jing H, Tai Y, Xu D, et al. Renal cell carcinoma associated with Xp11.2 translocations, report of a case [published online ahead of print October 23, 2009]. Urology. doi: / j.urology Lopez-Beltran A, Scarpelli M, Montironi R, et al WHO classification of the renal tumors of the adults. Eur Urol. 2006;49: Martignoni G, Pea M, Gobbo S, et al. Cathepsin-K immunoreactivity distinguishes MiTF/TFE family renal translocation carcinomas from other renal carcinomas. Mod Pathol. 2009; 22: Argani P, Ladanyi M. Recent advances in pediatric renal neoplasia. Adv Anat Pathol. 2003;10: Argani P, Lal P, Hutchinson B, et al. Aberrant nuclear immunoreactivity for TFE3 in neoplasms with TFE3 gene fusions: a sensitive and specific immunohistochemical assay. Am J Surg Pathol. 2003;27: Dickson BC, Brooks JS, Pasha TL, et al. TFE3 expression in tumors of the microphthalmia-associated transcription factor (MiTF) family [published online ahead of print February 16, 2010]. Int J Surg Pathol. doi: v Geller JI, Dome JS. Local lymph node involvement does not predict poor outcome in pediatric renal cell carcinoma. Cancer. 2004;101: Geller JI, Argani P, Adeniran A, et al. Translocation renal cell carcinoma: lack of negative impact due to lymph node spread. Cancer. 2008;112: Bovio IM, Allan R, Oliai B, et al. Xp11.2 translocation renal carcinoma with placental metastasis: a case report [published online ahead of print January 22, 2009]. Int J Surg Pathol. doi: v Koie T, Yoneyama T, Hashimoto Y, et al. An aggressive course of Xp11 translocation renal cell carcinoma in a 28-year-old man. Int J Urol. 2009;16: Jadad AR, Moore RA, Carroll D, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials. 1996;17: Kjaergard LL, Villumsen J, Gluud C. Reported methodologic quality and discrepancies between large and small randomized trials in meta-analyses. Ann Intern Med. 2001;135: Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21: Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327: Ramphal R, Pappo A, Zielenska M, et al. Pediatric renal cell carcinoma: clinical, pathologic, and molecular abnormalities associated with the members of the mit transcription factor family. Am J Clin Pathol. 2006;126: Wu A, Kunju LP, Cheng L, et al. Renal cell carcinoma in children and young adults: analysis of clinicopathological, immunohistochemical and molecular characteristics with an emphasis on the spectrum of Xp11.2 translocation-associated and unusual clear cell subtypes. Histopathology. 2008;53: Rao Q, Chen YJ, Wang DJ, et al. Renal cell carcinoma in children and young adults: clinicopathological, immunohistochemical, and VHL gene analysis of 46 cases with follow-up [published online ahead of print December 24, 2009]. Int J Surg Pathol. doi: v1.

7 464 International Journal of Surgical Pathology 18(6) 21. Moher D, Pham B, Jones A, et al. Does quality of reports of randomised trials affect estimates of intervention efficacy reported in meta-analyses? Lancet. 1998;352: Srigley JR, Delahunt B. Uncommon and recently described renal carcinomas. Mod Pathol. 2009;22(suppl 2):S2-S Rais-Bahrami S, Drabick JJ, De Marzo AM, et al. Xp11 translocation renal cell carcinoma: delayed but massive and lethal metastases of a chemotherapyassociated secondary malignancy. Urology. 2007;70:178. e3-e6.

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