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© 2002 American Society for Clinical Oncology Children From Ethnic Minorities Have Benefited Equally as Other Children From Contemporary Therapy for Rhabdomyosarcoma: A Report From the Intergroup Rhabdomyosarcoma Study GroupFrom the University of Minnesota, Minneapolis, MN; University of Nebraska Medical Center, Omaha, NE; LeBonheur Children’s Medical Center, Memphis, TN; Johns Hopkins Oncology Center, Baltimore, MD; Columbus Children’s Hospital, Columbus, OH; M.D. Anderson Cancer Center, Houston, TX; Children’s Hospital of Philadelphia, Philadelphia, PA; University of Oklahoma Health Sciences Center, Oklahoma City, OK; Stanford University Medical Center, Stanford, CA; and University of Missouri-Columbia University of Missouri, Columbia, MO. Address reprint requests to K. Scott Baker, MD, Children’s Oncology Group Operations Center, Publications Office, 440 E Huntington Dr, Arcadia, CA 91066-6012; email: baker084{at}tc.umn.edu
PURPOSE: To define the clinical characteristics of rhabdomyosarcoma (RMS) occurring in children from ethnic minorities and determine whether these children have benefited equally from advances in therapy. PATIENTS AND METHODS: This was a retrospective cohort analysis of children treated on the Intergroup Rhabdomyosarcoma Study Group protocols between 1984 and 1997. The clinical features and outcomes of 336 African-American children and 286 children from other ethnic minorities were compared with those of white children (n = 1,721). RESULTS: African-American, other ethnic group, and white children enjoyed similar 5-year failure-free survivals (FFS) of 61%, 61%, and 66%, respectively, P = .15. Compared with white children, nonwhite patients more often had (1) invasive, T2 tumors (P = .03); (2) stage 2 or 3 tumors (P = .003); (3) large tumors (more than 5 cm, P < .006); and/or (4) tumors with positive regional nodes (ie, N1, P = .002). Using Cox proportional hazards analysis, seven patient risk categories were defined with significant differences in outcome. This model was then used to search for other factors associated with FFS after adjusting for these risk categories. Only T stage and age remained associated with FFS (P = .001 and P < .001, respectively). After adjusting for T stage, risk category, and age, we explored the relationship of ethnic group to FFS and found that, compared with whites, the relative risk of failure was 1.14 for African-American patients and 1.2 for other ethnic minority patients, values that are not significantly different. CONCLUSION: Patients from ethnic minority groups more often have larger, invasive tumors with positive lymph nodes. Nevertheless, they have benefited as equally as white children from the dramatic progress in therapy of RMS.
CHILDHOOD CANCER IS the major cause of death from disease in children less than 15 years of age. Approximately 8% of childhood cancer is rhabdomyosarcoma (RMS), making this the most common soft tissue sarcoma in children. The cure rate for children with RMS has improved significantly during the past 30 years, primarily attributable to advances in therapy and supportive care. The Intergroup Rhabdomyosarcoma Study Group (IRSG, now the Soft Tissue Sarcoma Committee of the Children’s Oncology Group) has designed and conducted four consecutive clinical trials in the United States (IRS-I, 1972 to 1978; IRS-II, 1978 to 1984; IRS-III, 1984 to 1991; and IRS-IV, 1991 to 1997), which have demonstrated in a tripling of the cure rate for children with RMS from approximately 25% in 1970 to over 75% now.1-5
Previous analyses of IRSG data have demonstrated that stage, group, age, and histology can be used to define patient subgroups with differing outcome.1-4,6-8 Staging is based on the tumor-node-metastasis system and is determined by tumor location, size, and nodal involvement. Patients with tumors in favorable sites (including the orbit, nonparameningeal head and neck, and genitourinary [not bladder or prostate]) fare better than do patients with tumors at all other sites. Those with tumors Race is another potentially important patient characteristic that may carry prognostic significance. In many of the common types of cancer in adults (eg, prostate, breast, endometrium, colon, lung, Hodgkin’s disease, and acute myeloid leukemia), a survival disadvantage has been identified for African Americans.9-14 However, the impact of a patient’s race has never been adequately examined to date in children with RMS. Because of this potential prognostic importance of ethnic group, we reviewed the experience of the IRSG and herein report our data on an analysis of over 2,000 African-American, white, and other racial minority children with RMS, comparing disease status at time of diagnosis, prognostic features, and survival in the context of treatment on contemporary IRSG protocols (IRS-III, IRS-IV pilot, and IRS-IV).
Patients Eligible patients (n = 2,343) with embryonal, alveolar, or undifferentiated RMS who were entered onto successive IRSG protocols IRS-III, IRS-IV pilot, and IRS-IV between 1984 and 1997 were used for this analysis of outcome by race. There were 336 African-American children, 286 children from other ethnic minorities (Hispanic, 34%; Asian, 48%; and other, 18%), and 1,721 white children who were treated on these studies. All patients were previously untreated, younger than 21 years of age at diagnosis, and had a pathologically confirmed diagnosis of RMS or undifferentiated sarcoma. Patients were required to begin therapy within 42 days of the initial surgical procedure giving the definitive diagnosis. The protocols were approved by the institutional review boards of participating centers, and informed consent for participation was obtained from the parents or legal guardian, and when applicable, from the patient.
Patients were randomized to various treatment strategies based on their pretreatment stage, which is based on tumor site (favorable or other), size (
In IRS-III, therapy was determined by clinical group, site of tumor (stage), and histology (embryonal-favorable, alveolar/undifferentiated-unfavorable). Therapy for group I tumors of favorable histology (FH) consisted of cyclic-sequential vincristine and dactinomycin (VA) for 1 year. Patients with group II, FH tumors were randomized between VA + radiation therapy (RT) versus VA + doxorubicin (ADR) + RT, both given for 1 year. Group III and IV tumors (FH and unfavorable histology, except for group III, FH, and orbit and nonparameningeal head tumors) were randomized to one of the following three regimens given for 2 years with RT: (1) pulsed VA + cyclophosphamide (VAC), (2) pulsed vincristine (V) + ADR-VAC + cisplatin (CDDP), or (3) pulsed VADRC-VAC + CDDP + etoposide. Exceptions to this general treatment schema were made for certain special categories defined by clinical group, tumor site, and histology; these as well as other specific details of IRS-III therapy have been published previously.1 The IRS-IV pilot studies were designed to provide experience with new chemotherapy regimens for the treatment of patients with clinical group III RMS and to test the feasibility of hyperfractionated RT used in combination with these regimens. The pilot treatments included VAC with a dose escalation of cyclophosphamide, and two new regimens, VA + ifosfamide (VAI), and vincristine, ifosfamide, and etopside (VIE). Patients with group IV disease received induction with ifosfamide + doxorubicin, followed by VAC chemotherapy. The duration of therapy was 50 weeks. Details of each of these protocols have been reported.15-18 In IRS-IV, most patients with nonmetastatic RMS were randomized to receive one of three chemotherapy regimens from the pilot studies, VAC, VAI, or VIE, in a phase III randomized trial. Patients with group I paratesticular tumors or group I/II orbit/eyelid tumors, shown in previous studies to have an excellent outcome with VA chemotherapy, were assigned to receive those two drugs. For patients on the VAI or VIE treatment regimens, the total dose of ifosfamide was limited to 72 g/m2 to reduce renal toxicity. Cyclophosphamide replaced ifosfamide in the last four courses of therapy. Patients with stage 4 tumors were randomized to receive either vincristine + melphalan with VAC, or ifosfamide + etoposide with VAC. Therapy for patients with stage 1 or 2, group I tumors did not include RT. Conventional RT was given to patients with stage 2 or 3, group II tumors and to those with stage 3, group I tumors. All patients with group III tumors, with the exception of patients with vagina or vulva primary tumors, were eligible for randomization to conventional or hyperfractionated RT. These and other specific details of IRS-IV therapy have been previously published.5,7
Protocol guidelines for patient follow-up required that they be evaluated by the treating oncologist every 1 to 2 months for the first year after completion of therapy, every 3 months for the second year, every 6 months for the third year, and annually thereafter. Appropriate radiographic imaging studies after completion of therapy were suggested every 6 months for 2 years and then yearly for 2 additional years. Specific posttherapy data collection forms were submitted to the IRSG operations office, and date of recurrence or death from any cause for all patients on study were also reported.
Failure-free survival (FFS) was defined as the time from study registration to the first occurrence of progression, relapse after response, or death from any cause. Survival was defined as the time from study registration to death, again from any cause. Patients not experiencing the events of interest were censored at their time of last follow-up. Estimates of the distribution of time to events were computed using the Kaplan-Meier method.19 Comparisons of distributions of time to event among subsets of patients were made using the log-rank test. A Cox proportional hazards model20 was used to define risk categories with significant differences in outcome that were then entered into the model as strata. After adjusting for these risk categories, other factors were assessed as predictive for FFS (primary site of disease, clinical nodal status, primary tumor size, T stage, age, and sex). The prognostic significance of race was then assessed after adjustment for risk category and other significant factors.
Patient Characteristics and Follow-Up Patient characteristics by racial group (white, African-American, and other) are listed in Table 1. There were no statistically significant differences among the race categories for the distributions of sex, age, pathology, or group. However, we found that nonwhite patients more often had invasive T2 tumors (P = .03), tumors with positive regional lymph nodes (N1, P = .002), large tumors more than 5 cm (P = .006), and tumors which were stage 2 or 3 (P = .03) compared with white children. African-American patients also more often had tumors arising in the extremity or paratesticular sites (P = .003). Median follow-up for surviving patients was 4.9 years. Overall, 67% of surviving patients had last contact dates within 2 years of the timing of the analysis and an additional 12% within 3 years. Currency of follow-up (less than 2 years) by race was similar for white and African-American groups (69% and 65%, respectively), and in the other category it was similar for Hispanics (73%) but lower for Asians (46%).
Survival by Race Kaplan-Meier estimations of 5-year FFS were performed for each racial subgroup. No statistically significant difference in outcome could be found between white, African-American, or other minority patients (5-year FFS: 66%, 61%, and 61%, respectively; P = .15; Fig 1).
Prognostic Significance of Race Using Cox proportional hazards analyses we were able to define seven risk categories with significant differences in outcome. These categories and the 5-year FFS for each are shown in Table 2. A Cox proportional hazards model was again used in an attempt to identify other factors that might be predictive for FFS after adjusting for these seven risk categories. The risk categories were entered into the Cox model as strata and other risk factors such as T stage (locally invasive [T2] or not [T1]), clinical node status (involved or not), tumor size (size  or > 5 cm), sex, primary site, and age were analyzed for association with FFS after adjusting for these risk categories. From this analysis, no association with FFS was found for primary site of disease, clinical node status, tumor size, or sex. However, higher T stage (T2) was predictive for FFS (P = .001), as was the age of the patient (age less than 1 year, 1 to 9 years, or 10+ years; P < .001).
After adjusting for risk category, T stage, and age category, we then assessed the relationship of racial group to FFS outcome. From this, the relative risk of failure for African-American patients was 1.14, and for other ethnic minorities, the relative risk of failure was 1.20. Neither of these differences reached statistical significance (P = .24 and P = .13, respectively).
The examination of racial differences in the outcome of modern cancer therapy is important from both a biologic and social context. In childhood RMS, past studies have identified several biologic features that are important prognostically, and some of these form the basis for the current risk group definitions that determine the intensity of treatment for a particular patient. However, given the heterogeneity of RMS, it is likely that there are many biologic factors that we have yet to learn about. Whether an individual’s ethnic background has an impact (positive or negative) in RMS has not been looked at previously. If racial differences in outcome are discovered, it is important to try and determine whether there are biologic or nonbiologic explanations, such as barriers to accessing medical care, socioeconomic status, or cultural reasons, that these differences exist. Our finding that children and adolescents from ethnic minorities with RMS fare as well as do other children is gratifying. It clearly indicates that modern multimodal therapy has equally benefited all racial subgroups and underscores the importance of access to such treatments. Overall, more than one half of children with RMS in North America enter IRSG trials. No specific data regarding the outcome of other patients are available, but Surveillance, Epidemiology, and End Results (SEER) data suggest that survival for all patients with RMS in the United States has improved similarly over this time period.21 We did determine that there were notable ethnic differences identified in certain patient characteristics. We found that African-American and other ethnic minorities were more likely to have T2 tumors, clinical nodal involvement, and large (more than 5 cm) tumors at diagnosis. These characteristics are all indicative of more advanced disease at the time of diagnosis. Additionally, we did find that African Americans have more extremity and paratesticular tumors than did whites or other ethnic minorities. It is impossible for us to determine the reasons for these differences from our data. Because overall outcome remains the same, it seems unlikely that they are based on biologic differences in these tumors among racial subgroups. Other studies have examined inherent biologic differences between racial subgroups in tumor presentation, histology, stage at diagnosis, response to therapy, and other factors. For example, African-American males with prostate cancer have higher rates of metastatic disease and more advanced stage tumors at diagnosis.22-24 Similar findings have been reported for carcinoma of the breast,25,26 endometrium,27 colon,11 and for oral cancers.28 However, no study to date has clearly identified any specific biologic factor to explain these differences in presentation. There is evidence that for children with leukemia biologic factors may influence response to therapy and outcome. Investigators from the Pediatric Oncology Group have reported that African-American and Hispanic (Spanish surname) patients were more likely to have adverse prognostic features at diagnosis and lower survival than were white patients.29 Adjusting for age, leukocyte count, sex, era of treatment, and leukemia blast cell ploidy, they found that African-American children had a 42% excess mortality rate compared with white children, and Hispanic children had a 33% excess mortality rate compared with white children. Clinical presentation, tumor biology, and deviations from prescribed therapy did not explain the differences in survival and event-free survival that were observed, although differences seemed to be diminishing over time with improvements in therapy. These authors also conclude that disparity in outcome is most likely related to variations in response to chemotherapy and not to issues regarding compliance. Glutathione S-transferase (GST) is an enzyme involved in the metabolism of multiple different chemotherapeutic agents, and genetic polymorphisms of GST-T1 and GST-MI genes could potentially play a role in determining the cytotoxicity of these chemotherapeutic agents. In a study examining glutathione S-transferase polymorphisms and the outcome of childhood acute myeloid leukemia, Davies et al30 found that children who lacked the GST-T1 had greater toxicity and reduced survival after chemotherapy for acute myeloid leukemia compared with children with at least one GST-T1 allele. In this study, African-American race was associated with inferior outcome, but this was independent of GST genotype. Thus, although these studies reveal an inferior outcome for ethnic minority children, the exact reason for this cannot be determined. Certainly genetic differences in response to and tolerability of chemotherapeutic agents needs to be further evaluated, particularly to see if they play any role in a differential therapeutic response to treatment for RMS. We must also keep in mind that for RMS, treatment rarely includes chemotherapy alone. The surgical and RT interventions, and advances that have been made in those disciplines, are an extremely important part of the total treatment delivered and less likely to be affected by biologic factors. There are other factors that may have influenced the racial differences in patient characteristics observed. Cultural attitudes in seeking medical care as well as the potential lack of access to primary care (and subsequently delayed diagnosis) for ethnic minorities may have contributed to this finding. Socioeconomic status has been evaluated as a contributing factor to racial differences in outcome for cancer patients. However, even controlling for stage of disease, most studies suggest that socioeconomic status alone cannot explain a racial difference in outcome.9,10,31,32 Most published literature on racial outcomes in pediatric cancer therapy has been studies in leukemia, and there is a much smaller literature examining racial differences in outcomes for pediatric solid tumors. The most significant analysis was published in 1995 from St Jude Children’s Research Hospital, which reviewed their 30-year experience on the outcome of treatment for cancer in African-American as compared with white children.33 This analysis determined that, for the recent treatment eras, there was no significant difference in survival among racial groups for all cancers combined or when stratified by disease. However, African-American children from the early treatment era in this study with acute lymphoblastic leukemia did poorly. Other studies from the early 1980s demonstrated that African-American children with acute lymphoblastic leukemia were more likely to have unfavorable prognostic features at diagnosis.34,35 However, in the St Jude experience as well as in other reports, with current intensified therapy and risk-directed protocols, there is no longer a difference in outcome for these patients.35,36 It is important to note that our data pertain only to those patients who received protocol-directed IRSG therapy, which, by and large, is administered in academic medical centers or children’s hospitals by pediatric oncologists. Thus, we cannot comment about racial differences in outcome for children with RMS who are not treated on these protocols. We do know, however, that 94% of children less than 15 years of age diagnosed with cancer in the United States are treated on cooperative group protocols when they are available, and that the racial distribution of minorities on those protocols does not notably differ from the expected distribution based on the cancer incidence in the United States.37 However, only 21% of expected adolescent patients (ages 15 to 19) were registered on these protocols. Based on comparisons to SEER data, the racial distribution of RMS cases on IRSG studies very closely parallels that of RMS cases in the United States general population.21 Comparing SEER incidence rates by race over the time period of the IRS-III and IRS-IV studies with the number of cases actually enrolled onto these studies, we can demonstrate that the enrollment onto IRS studies accounted for approximately 50% of the whites, 50% of the African Americans, and 74% of other ethnic minorities aged 1 to 19 who were diagnosed with RMS over the time period of these studies. During accrual to IRS-IV (1991 to 1997), 65% of the expected cases ages 0 to 9 years were registered onto the study, whereas the proportions for ages 10 to 14 and ages 15 to 19 were 60% and 40%, respectively. Thus much of the under-enrollment on IRS studies occurs in the adolescent age group and does not seem to be due to racial under-representation. From this analysis, we have determined that race has not been a prognostic factor for children with RMS when corrected for stage and clinical group and that children of ethnic minorities have benefited as equally as white children from contemporary therapy for RMS such that their overall outcomes are equivalent. However, additional studies will be required to investigate the reasons (social or biologic) why children of ethnic minorities have several significant differences in clinical features at diagnosis from white children. In view of these encouraging findings, we recommend efforts to ensure equal access to therapy, and the enrollment of children (particularly adolescents) with RMS on clinical trials in the United States should continue.
Supported by Department of Health and Human Services, United States Public Health Service grant nos. CA24507, CA-30138, CA-30969, CA-29139, and CA-13539. We acknowledge members of the Soft Tissue Sarcoma Committee of the Children’s Oncology Group, Arcadia, CA, including Richard J. Andrassy, MD, Carola Arndt, MD, Frederic G. Barr, MD, W. Archie Bleyer, MD, Philip Breitfeld, MD, John C. Breneman, MD, Julia Bridge, MD, Kenneth L.B. Brown, MD, Holcombe E. Grier, MD, Douglas Hawkins, MD, Peter J. Houghton, PhD, Karen Lindsley, MD, Harold M. Maurer, MD, Jeff Michalski, MD, Sharon Murphy, MD, Charles N. Paidas, MD, Alberto S. Pappo, MD, David M. Parham, MD, Leslie Robison, PhD, Eric Sandler, MD, Lynn Smith, MD, Poul H.B. Sorensen, MD, PhD, Lisa Teot, MD, Timothy Triche, MD, PhD, Teresa J. Vietti, MD, David Walterhouse, MD, and Eugene S. Wiener, MD. The acknowledgment is available online at www.jco.org.
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5. Crist WM, Anderson JR, Meza JL, et al: Intergroup Rhabdomyosarcoma Study-IV: Results for patients with nonmetastatic disease. J Clin Oncol 19: 3091-3102, 2001 6. Lawrence W Jr, Anderson JR, Gehan EA, et al: Pretreatment TNM staging of childhood rhabdomyosarcoma: A report of the Intergroup Rhabdomyosarcoma Study Group. Children’s Cancer Study Group. Pediatric Oncology Group. Cancer 80: 1165-1170, 1997[CrossRef][Medline]
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24. Kim JA, Kuban DA, el-Mahdi AM, et al: Carcinoma of the prostate: Race as a prognostic indicator in definitive radiation therapy. Radiology 194: 545-549, 1995 25. Ownby HE, Frederick J, Russo J, et al: Racial differences in breast cancer patients. J Natl Cancer Inst 75: 55-60, 1985[Medline]
26. Eley JW, Hill HA, Chen VW, et al: Racial differences in survival from breast cancer: Results of the National Cancer Institute Black/White Cancer Survival Study. JAMA 272: 947-954, 1994 27. Hill HA, Eley JW, Harlan LC, et al: Racial differences in endometrial cancer survival: The black/white cancer survival study. Obstet Gynecol 88: 919-926, 1996[CrossRef][Medline] 28. Arbes SJ, Slade GD: Racial differences in stage at diagnosis of screenable oral cancers in North Carolina. J Public Health Dent 56: 352-354, 1996[Medline]
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30. Davies SM, Robison LL, Buckley JD, et al: Glutathione S-transferase polymorphisms and outcome of chemotherapy in childhood acute myeloid leukemia. J Clin Oncol 19: 1279-1287, 2001 31. Franzini L, Williams AF, Franklin J, et al: Effects of race and socioeconomic status on survival of 1,332 black, Hispanic, and white women with breast cancer. Ann Surg Oncol 4: 111-118, 1997[CrossRef][Medline]
32. Lannin DR, Mathews HF, Mitchell J, et al: Influence of socioeconomic and cultural factors on racial differences in late-stage presentation of breast cancer. JAMA 279: 1801-1807, 1998
33. Pui CH, Boyett JM, Hancock ML, et al: Outcome of treatment for childhood cancer in black as compared with white children: The St Jude Children’s Research Hospital experience, 1962 through 1992. JAMA 273: 633-637, 1995 34. Kalwinsky DK, Rivera G, Dahl GV, et al: Variation by race in presenting clinical and biologic features of childhood acute lymphoblastic leukaemia: Implications for treatment outcome. Leuk Res 9: 817-823, 1985[CrossRef][Medline] 35. Evans WE, Rodman J, Relling MV, et al: Individualized dosages of chemotherapy as a strategy to improve response for acute lymphocytic leukemia. Semin Hematol 28: 15-21, 1991[Medline] 36. Pui CH, Ribeiro RC, Hancock ML, et al: Acute myeloid leukemia in children treated with epipodophyllotoxins for acute lymphoblastic leukemia. N Engl J Med 325: 1682-1687, 1991[Abstract] 37. Bleyer WA, Tejeda H, Murphy SB, et al: National cancer clinical trials: Children have equal access; adolescents do not. J Adolesc Health 21: 366-373, 1997[CrossRef][Medline] Submitted November 27, 2001; accepted July 23, 2002.
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Copyright © 2002 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
