Acute Lymphoblastic Leukemia in Children: A Fifteen Year Experience at the Princess Nourah Oncology Center, Jeddah, Saudi Arabia.

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1 Acute Lymphoblastic Leukemia in Children: A Fifteen Year Experience at the Princess Nourah Oncology Center, Jeddah, Saudi Arabia. 1 Dr. C. Fryer FRCP(C), 2 Dr. S. Felimban FACHARTZ, 3 C. Paltiel MS 4 Dr. T. Khattab MD, 5 Dr A. Abbas MRCPCH, 6 Dr A. Yousef MS 1 BC s Children s Hospital, Room A119A, 4480 Oak St, Vancouver, B.C. Canada, V6H 3V4 2 Princess Nourah Oncology Center, King Abdulaziz Medical City, P.O. Box 9515, Jeddah, Kingdom of Saudi Arabia, Population and Preventive Oncology, British Columbia Cancer Agency, 600 West 10 th Avenue, Vancouver British Columbia, Canada. V5Z4E6 4 Princess Nourah Oncology Center, King Abdulaziz Medical City, P.O. Box 9515, Jeddah, Kingdom of Saudi Arabia, Department Clinical Heamtology/Oncology, Women s and Children s Hospitalm, 72 King Williams Road North Adelaide, Australia, SA Princess Nourah Oncology Center, King Abdulaziz Medical City, P.O. Box 9515, Jeddah, Kingdom of Saudi Arabia, ABSTRACT We evaluated NCI risk and therapy on survival (S) in 308 children age <15yrs with acute lymphoblastic leukemia diagnosed from Five and 10 yr. S was 74% and 64%. Standard risk (SR) patients had 80% 5 yr. S vs. 64% for high risk (HR) (p<0.0001). The 36 T-cell patients had a 27% 5 yr. S. Improvements were associated with more intensive therapy. SR patients treated with UKALL X and a single intensification fared worse than those receiving UKALLXI/BFM or MRC ALL97/ CCG1991 therapy. Improvements in HR patients occurred using MRC ALL97 and CCG 1991 protocols. Keywords: childhood lymphoblastic leukemia, prognosis. INTRODUCTION While white blood cell count (WBC) and age at diagnosis are major factors in stage and risk classification in childhood acute lymphoblastic leukemia (ALL), therapy remains the single most important prognostic factor. 1, 2 The recognition that delayed intensification, pioneered by Riehm, improves outcome, led many groups to adopt a risk based management approach. 3-6 The Princess Nourah Oncology Center (PNOC) is a major referral center for Saudi children with cancer living in western and southern Saudi Arabia. The referral area covers more than 350,000 Km 2, with sparse primary pediatric care facilities, presenting a significant challenge in childhood cancer management. We wished to assess whether the current NCI risk categories for ALL are the most appropriate in our patient population. We also wanted to evaluate the effect of newer therapies and to ascertain whether a risk based approach was justifiable in our patient population. Correspondence to: Christopher J.H. Fryer, Clinical Professor, Division Pediatric Hematology/Oncology/BMT, Department of Pediatrics, Children s & Women s Health Centre of British Columbia, 4480 Oak St. Room A 119A, Vancouver B.C., Canada V6H 3V4. cfryer@cw.bc.ca Austral - Asian Journal of Cancer ISSN , Vol. 5, No.4, October

2 Christopher J.H. Fryer METHODS Data We undertook a retrospective review of all ALL patients age < 15 years (yr) referred to the pediatric oncology division at the PNOC from Information regarding age, sex, WBC and phenotype at diagnosis was recorded, as well as initial treatment, relapse data and status. Chromosomal data and day 7 or day 14 bone marrow status was not evaluated. Patients were grouped into known risk groups for age (< 1yr; yr; yr; 10+yr), WBC (<10; ; ; ; 100+; x 10 9 /L) and phenotype (Pre-B; T-cell). Patients were also grouped according to the NCI classification and a local classification that included all T-cell patients in the NCI high risk category. 1 Incomplete data Where data was incomplete patients were excluded from that analysis. Infants (age<1 yr) were analyzed separately. Analyses were based on 5 yr survival rates (S) since the relapse date was often unavailable. Treatment The therapies used were modifications of established protocols and varied with the different eras (Table1). These protocols and their modifications have been published previously. 6-9 In general, patients with NCI high risk and T- cell patients were treated on the more intensive arms (Table 1). In 1999 all patients received MRC ALL97 therapy with dexamethasone instead of prednisone and three intensifications. In 2001 we adopted the CCG 1991 Regimen OD with double delayed intensification for our standard risk patients and augmented BFM with a four drug induction for our high risk patients. Initially daunomycin was given on day 0 but this was subsequently changed to day 14. Definitions Induction deaths were defined as deaths occurring within the first 30 days. Deaths from toxicity were defined as deaths occurring while in 1 st complete remission. All other deaths were due to disease. Statistics Patient characteristics were compared to data published on large series of children with ALL. Standard life table methods and associated statistical tests were employed for analysis of outcome. 10 Survival information was calculated from diagnosis to relapse or death. Disease specific survival was calculated on the basis that deaths in induction or from toxicity were censored at the time of death. The relationships between the baseline characteristics of age group, WBC, sex, immunophenotype, era of treatment and treatment protocol, and the overall survival outcome, were analyzed using Kaplan-Meier survival curves and log-rank tests to measure significance. Analyses within defined risk groups were also performed. RESULTS Missing Data Data on initial WBC was missing in 10 patients, and data on phenotype was unavailable in 39. The missing data was mainly in the earliest era. Patient Characteristics and Survival A total of 308 patients were seen during the study period. Eleven patients were age < 1 yr at diagnosis and are analyzed separately. Thirteen patients had central nervous system involvement at diagnosis. The presenting characteristics and the corresponding 5 and 10 yr survival rates (S) of the remaining 297 patients are seen in Table 2. The overall 5 yr Table 1. Protocols used Era NCI Standard Risk non T-cell NCI High Risk or T-cell UKALLX REG B ( single early UKALL X REG D intensification two intensifications UKALL XI 3 Intensifications ALL-BFM MRC ALL97 with dexamethasone MRC ALL97 with dexamethasone and 3 intensifications and 3 intensifications CCG 1991 Delayed Intensification x 2 CCG 1991 Aug BFM 200

3 Acute Lymphoblastic Leukemia in Children: A Fifteen Year Experience... Table 2. Presenting Characteristics and 5 and 10 year Survival Patient Characteristics # of Pts % 5 yr S SE 10 yr S SE p Overall Survival 297 (100%) 74% % 4.1 Disease Specific Survival 297 (100%) 82% % 4.1 Sex Female 132 (44%) 72.6% % 5.9 } Male 165 (56%) 75.3% % 5.6 } N.S Age yrs 152 (51%) 83% % 5.2 See text yrs 105 (35%) 65.7% % yrs 40 (14%) 63% % 12.5 WBC ( 10 unknown) <10 x 10 9 /L 148 (50%) 81% % 4.8 See text x 10 9 /L 32 (11%) 82.3% % x 10 9 /L 52 (17.5%) 75% % x 10 9 /L 24 (8%) 60.8% % x 10 9 /L 31 (10%) 57.6% % 10.6 Phenotype (39 unknown) T-Cell 36 (12%) 27.3% % 7.9 } Pre-B 222 (75%) 83.6% % 5.7 }< NCI Risk (9 unknown) High Risk (HR) 84 (28%) 63.8% % 8.4 } Standard Risk (SR) 204 (69%) 80.3% % 4.4 }< PNOC risk (29 unkown) NCI HR or T-cell 104 (35%) 57.2% % 7.5 } NCI SR non T-cell 164 (55.2%) 86.4% % 5.4 }< PNOC SR Subclassification Medium Risk 82 (50%) 82.7% % 8.0 } Low Risk 82 (50%) 90.5% % 7.0 }N.S Year of Diagnosis (24%) 56.7%** % 6.2 }** 5 yr (32%) 73% ** % 9.1 }< (44%) 86.5%** 3.4 N/A } Protocol UKALL X ( 89-93) 67 (23%) 55.5% % 6.5 } UKALL XI/BFM( 94-98) 98 (33%) 72.8% % 8.4 }< MRC/CCG comb ( 99-03) 132 (44%) 86.7% 3.3 n/a } MRC 97 ( 99-00) 45 (15%) 86.7% 5.1 n/a Mod.CCG1991 ( 01-03) 87 (29%) 88.5%* 3.6 n/a *3Yr Survival. NS=Not significant. Subclassification:Medium Risk =age WBC x 10 9 /L or age yr +WBC <50 x 10 9 /L. Low Risk = age1-4.99yr +WBC<20 x 10 9 /L 201

4 Christopher J.H. Fryer survival was 74%. There was a steady improvement in 5 yr S over the different eras and this correlated closely with the different therapies given. Effect of age In this study there was no significant difference in overall survival in patients age yr (5 yr S 65.7%) compared to patients age yr (5 yr S 63%). However, both of these age groups fared worse than patients age yr (5 yr S 83%) (pairwise log-rank test p-values of.003 and.014 comparing the elder and middle age groups respectively to the youngest). Effect of WBC When patients were categorized into groups based on WBC, a trend of higher values being correlated with lower survival is seen in the Kaplan-Meier survival graphs (Table 2). However the only significant pairwise comparison was between the lowest concentration and the highest. Using the NCI criteria, patients with WBC< 50 x 10 9 /L had a 79% 5 year S vs 55% for WBC>50 x 10 9 /L (p< for log-rank test). patients in the PNOC defined low risk group (non T-cell) with an 86% 5year S compared to 57% for the high risk group (Table2). We identified a subgroup of the lowest risk patients as those age yrs with WBC<20 x 10 9 /L. Although these patients had a better survival than the rest of the low risk group (5 year S of 91% vs 83%), the p-value of 0.24 indicates that the difference between them is not significant (Table 2). Effect of Treatment The overall 5yr survival improved from 55%for patients treated per UKALLX to 72% per UKALLXI/BFM and 87% per MRC ALL97/CCG1991 (Table2). Within each risk group we analyzed the impact of therapies on outcome. The results were similar using either the NCI or the PNOC risk criteria. Because the PNOC risk in 22/67 patients treated with the UKALL X protocol was unknown, we chose to use the NCI risk criteria. The distribution of NCI risk by treatment and corresponding 5year S is shown in Table 3. In the low risk patients the survival using the UKALL X protocol was significantly lower than the UKALL XI/ALL- BFM-90 and the combined MRC ALL97 and CCG1991 protocols (Figure 1). In the high risk patient group, those treated on the MRC ALL97 and CCG1991 protocols had a Table 3. Outcome for NCI risk group by treatment Treatment NCI High Risk NCI Low Risk Unknown # pts % 5yr S SE # pts %5yr S SE UKALL X UKALL XI/BFM MRC 97/ CCG NCI Risk Grouping Using the NCI prognostic criteria of age and WBC, there was insufficient data in 9 patients. In the remaining 288 cases the SR patients had a 5yr S of 80% compared to 64% for HR patients (p<0.001). In our T-cell group 17/36 were NCI high risk and 3/36 were NCI unknown risk. The T-cell patients fared extremely poorly with 5yr S of 27%. PNOC Risk Category Because phenotype remained a strong prognostic factor even after adjusting for age and WBC (p<0.0001), we included all T-cell patients in our PNOC high risk group. There were 29 patients (9.8%) who could not be classified by PNOC risk because of missing data. There were 164 significantly higher proportion surviving than those experiencing either the UKALL X or UKALLXI/ALL- BFM-90 therapy (Figure 2). Table 4 shows the pair-wise log-rank tests comparing treatments within the local risk groups. Causes of death Eight of 11 infants died including 4 during induction. There were 74 deaths among the remaining 297 patients. Fifty patients died of disease recurrence. Twelve deaths occurred during induction including 2 who died within the first 24hrs. Three of the recent induction deaths were attributable to Stenotrophomonas Maltaphilia. 11 An additional 11 patients died of toxicity, 6 during maintenance. One patient died in a car accident. When the deaths from 202

5 Acute Lymphoblastic Leukemia in Children: A Fifteen Year Experience... Figure 1. Survival for NCI Low Risk by Treatment Figure 2. Survival for NCI High Risk By Treatment Table 4. Log-rank Tests Comparing Treatment Groups within NCI Risk Categories Pairwise Comparisons UKALL X UKALL XI/BFM MRC/CCG comb NCI Risk newtrt Chi-Square Sig. Chi-Square Sig. Chi-Square Sig. Log Rank (Mantel-Cox) High Risk UKALL X UKALL XI/BFM MRC/CCG comb Standard Risk UKALL X UKALL XI/BFM MRC/CCG comb induction or toxicity were censored, the 5 year disease specific survival was 82%. DISCUSSION While we attribute the improvements in outcome to the use of more intensive therapies, it is possible that better salvage therapy may also be a factor, since we did not evaluate event free survival. The better outcome in the low risk patients was associated with the use of more than one intensification while the improvement in the high risk patients was associated with the substitution of dexamethasone for prednisone and included daunomycin as a fourth induction agent. Despite the improvement in our 5 yr S, the results are still inferior to larger series using similar protocols. 2,4-6,9,12 The distribution of prognostic factors, (age, sex, WBC and phenotype) is similar to these larger series, therefore alternative explanations must account for these outcome differences. Other issues to consider include the 4% induction mortality and the additional 11 deaths secondary to toxicity, resulting in an 8% difference between the overall survival and disease specific survival. Lack of a sophisticated primary health care system meant that sick patients would sometimes have to travel large distances to our center to receive care for treatment related complications such as bleeding and febrile neutropenia. In attempting to reduce these deaths we had previously reported that delaying insertion of central lines for more than three weeks from diagnosis did not influence the risk of infection. 7 We had shown that prophylactic ciprofloxacin during delayed intensification reduced the frequency of gram negative sepsis. 13 This approach might reduce some septic related deaths although in that study no deaths occurred during delayed intensification. While the outcome for patients we placed in the lowest risk group (non T-cell, age years, WBC < 20 x 10 9 /L) 203

6 Christopher J.H. Fryer was not statistically significantly different from other low risk patients there was a trend toward improved survival (90% vs.83%). The lack of significance may have been due to insufficient sample size. Using these criteria and excluding patients with chromosomal abnormalities that predict for poor outcome, as well as those patients identified by bone marrow examination as slow early responders, we hope to reduce therapy, thereby reducing treatment related mortality and improving survival. CONCLUSIONS Although the NCI risk classification is useful, careful analysis of local experiences needs to be undertaken to verify the appropriateness of selecting therapies based on this classification. REFERENCES 1 Smith M, Arthur D, Camitta B, Carroll A, et al. Uniform approach to risk classification and treatment assignment for children with acute lymphoblastic leukemia. J Clin Oncol 1996;14: Hann I, Harrison G, Harrison C, Eden O, etal. Determinants of outcome after intensified therapy of childhood lymphoblastic leukaemia:results from Medical Research Council United Kingdom acute lymphoblastic leukaemia XI protocol. B J Haematol 2001;113: Riehm H, Gadner H, Henze G, Langermann H-J,et al. The Berlin childhood acute lymphoblastic leukemia therapy study Am J Pediatr Hematol Oncol. 1980;2: Gaynon P, Trigg M, Heerema M, Sather H, et al. Children s Cancer Group trials in childhood acute lymphoblastic leukemia: leukemia 2000;14: Kamps W, Bokkerink J, Hahlen K, Hermans J, et al. Intensive treatment of children with acute lymphoblastic leukemia according to ALL-BFM-86 without cranial radiotherapy:results of Dutch Childhood Leukemia Study Group Protocol ALL-7 ( ) Blood 1999;15: Schrappe M, Reiter A, Ludwig W-D, Harbott J, et al. Improved outcome in childhood lymphoblastic leukemia despite reduced use of anthracyclines and cranial radiotherapy: results of trial ALL-BFM 90. Blood 2000;95: Abbas A, Fryer C, Paltiel C, Chedid F, et al. Factors influencing central line infections in children with acute lymphoblastic leukemia: results of a single institutional study. Pediatr Blood Cancer 2004;42: Chessels J, Bailey C, Richards S. Intensification of treatment and survival in all children with acute lymphoblastic leukaemia: results of UK Medical Research Council trial UKALL X. Medical Council Working Party on Childhood Leukaemia. Lancet 1995;345: Hann I, Vora A, Richards S, Hill F, et al. Benefit of intensified treatment for all children with acute lymphoblastic leukaemia: results from MRC UKALL XI and MRC AL97 randomized trials. Leukemia 2000;14: Kaplan E, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc.1958;53: Abbas A, Fryer C, Felimban S, Yousef A, et al. Stenotrophomonas maltophilia infection related mortality during induction in childhood acute lymphoblastic leukemia. Med Pediatr Oncol 2003;41: Maloney K, Shuster J, Murphy S, Pullen J, Camitta B. Longterm results of treatment studies for childhood acute lymphoblastic leukemia: Pediatric Oncology group studies from Leukemia 2000;14: Yousef A, Fryer C, Chedid F, Abbas A, et al. A pilot study of prophylactic ciprofloxacin during delayed intensification in children with acute lymphoblastic leukemia. Pediatr Blood Cancer 2004;43:

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