Original Article
Extended Follow-up of Long-Term Survivors of Childhood Acute Lymphoblastic Leukemia
N Engl J Med 2003; 349:640-649August 14, 2003
- Abstract
Background
Children who survive acute lymphoblastic leukemia are at risk for leukemia-related or treatment-related complications, which can adversely affect survival and socioeconomic status. We determined the long-term survival and the rates of health insurance coverage, marriage, and employment among patients who had attained at least 10 years of event-free survival.
Methods
A total of 856 eligible patients were treated between 1962 and 1992 in 13 consecutive clinical trials. Survival rates, the cumulative risk of a second neoplasm, and selected indicators of socioeconomic status were analyzed for the entire group and for patients who did or did not receive cranial or craniospinal radiation therapy during initial treatment.
Results
Fifty-six patients had major adverse events, including 8 deaths during remission, 4 relapses, and 44 second neoplasms (41 of them radiation-related); most of the second neoplasms were benign or of a low grade of malignant potential. The risk of a second neoplasm was significantly higher in the 597 patients who received radiation therapy (irradiated group) than in the 259 patients who did not receive radiation therapy (nonirradiated group) (P=0.04; estimated cumulative risk [±SE] at 20 years, 20.9±3.9 percent vs. 0.95±0.9 percent). The death rate for the irradiated group slightly exceeded the expected rate in the general U.S. population (standardized mortality ratio, 1.90; 95 percent confidence interval, 1.12 to 3.00), whereas that for the nonirradiated group did not differ from the population norm (standardized mortality ratio, 1.75; 95 percent confidence interval, 0.34 to 5.00). The rates of health insurance coverage, marriage, and employment in the nonirradiated group were similar to the age- and sex-adjusted national averages. Despite having health insurance rates similar to those in the general population, men and women in the irradiated group had higher-than-average unemployment rates (15.1 percent vs. 5.4 percent and 35.4 percent vs. 5.2 percent, respectively), and women in the irradiated group were less likely to be married (35.2 percent vs. 48.8 percent).
Conclusions
Children with acute lymphoblastic leukemia who did not receive radiation therapy and who have attained 10 or more years of event-free survival can expect a normal long-term survival. Irradiation is associated with the development of second neoplasms, a slight excess in mortality, and an increased unemployment rate.
Media in This Article
Figure 1
Mean (±SE) Cumulative Incidence of Any Adverse Event in Patients Attaining 10 or More Years of Event-free Survival.Figure 2
Mean (±SE) Cumulative Incidence of Second Neoplasms or Any Adverse Event among Patients Attaining 10 or More Years of Event-free Survival, According to Whether or Not They Received Cranial or Craniospinal Radiation.Article Activity
- Article
Acute lymphoblastic leukemia, the most common childhood cancer, is highly responsive to chemotherapy. Among patients receiving contemporary therapy, the overall five-year survival rate is 80 to 86 percent1,2 and the five-year event-free survival rate is 78 to 83 percent.3-5 Each year in the United States, approximately 2000 patients become five-year survivors of childhood acute lymphoblastic leukemia.6 Although most of these patients are likely to be cured, a substantial proportion will die of leukemic relapse, a second cancer, or some other treatment-related complication during the next five years of follow-up.7,8 Hence, long-term survivors of childhood acute lymphoblastic leukemia are still perceived by many to have an excessive risk of cancer or other catastrophic disease. This perception can lead to the denial of life insurance or health insurance or an offer of restricted or costly coverage.
Adverse events after treatment of acute lymphoblastic leukemia tend to occur within the first decade after diagnosis.7,8 We therefore sought to determine the prospects for normal survival among patients attaining at least 10 years of complete remission.
Methods
Study Population and Treatment Protocols
From 1962 through 1992, 2069 patients with acute lymphoblastic leukemia under 21 years of age were enrolled in 13 consecutive clinical trials (Table 1Table 1
General Characteristics of Treatment Protocols.)9-13 at St. Jude Children's Research Hospital in Memphis, Tennessee; 1112 patients survived for 10 years or more after the induction of remission. In this cohort of survivors, 856 who had no leukemic recurrence were considered eligible for the follow-up analysis.Follow-up Procedures
After the completion of therapy, all patients were examined at least annually at our center. Patients who had remained in remission for at least 10 years and were 18 years of age or older were subsequently monitored by their local physicians. The status of these patients was ascertained by questionnaires sent annually by the hospital's tumor registrar. The records of patients who died or had a second cancer were reviewed. Histopathological samples of second cancers were reviewed by St. Jude pathologists. For deaths outside the institution, death certificates were routinely requested, and the reported cause was verified by telephone conversations with the local physician, the family, or both. When available, reports of postmortem examinations were also reviewed. At the time of our analysis, only 44 patients (5.1 percent) lacked a documented contact within the previous three years; 599 (70.0 percent) had been contacted within the previous year. The median follow-up for patients attaining at least 10 years of event-free survival was 18.9 years (range, 10.0 to 38.6).
With the approval of the institutional review board, a questionnaire was mailed to all eligible patients who were at least 18 years of age to ascertain health insurance coverage and other socioeconomic characteristics. The results were compared with findings in the general population of the United States in 2000 and 2001.14-16
Statistical Analysis
Survival and event-free survival from the 10th anniversary date of event-free survival (base line) were estimated by the method of Kaplan and Meier, and the associated standard errors were calculated by the method of Peto and Pike.17 Survival estimates for different groups of patients were compared by a Cox proportional-hazards regression model adjusted for age at the diagnosis of leukemia, sex, race, and treatment era (studies 1 to 10 vs. studies 11 to 13). The duration of event-free survival was measured from base line to the date of the first treatment failure of any kind (relapse, second cancer, or death) or to the date of the last follow-up. Cumulative incidence functions for second cancers, relapses, and deaths during remission were analyzed by Gray's method18 and with use of a proportional-hazards model adjusted for age and leukocyte count at diagnosis.19
Standardized mortality ratios (the observed number of deaths divided by the expected number) and their 95 percent confidence intervals were calculated by the method of Breslow and Day.20 The expected number of deaths was calculated with the Epilog Plus Program21 by multiplying the number of person-years of follow-up by the corresponding mortality rate in the general population matched for age, sex, race, and calendar year (1973 to 2000) in which our patients achieved their first 10 years of event-free survival. Confidence intervals were calculated by Byar's approximation.20 The survival curve of the U.S. population was constructed as a linear interpolation of the expected survival for each year from 1973 to 2000. The expected survival in a calendar year was calculated as 1 minus the expected risk of death in that year, which was defined as the expected number of deaths in that year divided by the total number of patients at risk. The expected number of deaths in a calendar year was calculated by multiplying the number of patients at risk in that year by the average death rate in the U.S. population from 1973 to 2000, after adjustment for age, sex, and race.
The standardized incidence ratio, or the number of observed cases divided by the number of expected cases, for second cancers was calculated on the basis of data from the Surveillance, Epidemiology, and End Results (SEER) program, adjusted for age and sex. Confidence intervals were calculated by Byar's approximation or, in cases with two or fewer observed events, by the exact Poisson distribution.
The summary statistics and national average rates of marriage, employment, and health insurance coverage were stratified according to sex and age categories identical to those of the Medical Expenditure Panel Survey14 or the Current Population Surveys of the U.S. Census Bureau.15,16 Confidence intervals were calculated by exact multinomial statistics. The age-adjusted national average was calculated as the sum of the fraction of participants in each age category multiplied by the sex-specific rate of employment or marital status (Current Population Surveys) or by the insurance rate for that age category (Medical Expenditure Panel Survey). Multiple logistic-regression analysis was used to compare the rates of marriage, employment, and health insurance coverage between the patients who received cranial or craniospinal radiation therapy as part of their initial treatment (irradiated group) and those who did not receive such therapy (nonirradiated group), with adjustment for age and leukocyte count at the diagnosis of acute lymphoblastic leukemia, age at the time of survey, sex, and race. All reported P values are two-sided.
Results
Patient Characteristics
Of the 856 patients studied, 419 (48.9 percent) were male and 788 (92.1 percent) were white. Their ages ranged from 0.2 to 20 years (median, 4.5) at the time of diagnosis and from 10.3 to 30.2 years (median, 14.6) when they attained 10 years of event-free survival. The median leukocyte count at diagnosis was 8600 per cubic millimeter (range, 800 to 999,000). Of the 549 cases with successful immunophenotyping, 475 (86.5 percent) were classified as B-lineage acute lymphoblastic leukemia. Hyperdiploid karyotypes (more than 50 chromosomes) were identified in 195 of the 499 cases analyzed (39.1 percent).
Adverse Events
Fifty-six patients had adverse events after the 10th anniversary date of event-free survival (Table 2Table 2
Timing and Cumulative Risk of Adverse Events after the 10th Anniversary of Event-free Survival.). The cumulative incidence (±SE) of any adverse event was 5.1±0.9 percent at 10 years after base line (20 years after the induction of remission) and 22.0±3.8 percent at 20 years after base line (30 years after the induction of remission). When basal-cell carcinoma was excluded, these rates were 4.7±0.9 percent and 14.7±2.9 percent, respectively (Figure 1Figure 1Mean (±SE) Cumulative Incidence of Any Adverse Event in Patients Attaining 10 or More Years of Event-free Survival.). With three exceptions, the second neoplasms occurred within or adjacent to the field of cranial or craniospinal irradiation. Only one second neoplasm (Hodgkin's disease) was found among the 259 patients in the nonirradiated group.In a proportional-hazards regression model adjusted for age and leukocyte count at diagnosis, the 597 patients in the irradiated group had a significantly higher cumulative risk of second neoplasms than did the 259 patients in the nonirradiated group (P=0.04; estimated cumulative incidence rate at 20 years after base line, 20.9±3.9 percent vs. 0.95±0.9 percent) (Figure 2Figure 2
Mean (±SE) Cumulative Incidence of Second Neoplasms or Any Adverse Event among Patients Attaining 10 or More Years of Event-free Survival, According to Whether or Not They Received Cranial or Craniospinal Radiation.). By comparison with data from the SEER program, we determined that the risk of a second neoplasm was increased only in the irradiated group (Table 3Table 3
Comparison of the Incidence of Cancer in the Study Group with That in the General Population.). The irradiated group also appeared to be at greater risk for any adverse event (P=0.08; estimated cumulative risk rate at 20 years from base line, 23.0±3.8 percent vs. 2.7±1.4 percent) (Figure 2).Survival
At 20 years from base line (30 years from achievement of the first complete remission), the estimated survival rates for the entire group and the irradiated and nonirradiated groups were 95.3±2.2, 95.1±2.3, and 98.3±7.4 percent, respectively, as compared with 99.7 percent for the general U.S. population (Figure 3Figure 3
Overall Survival of the Entire Group of Patients Attaining 10 or More Years of Event-free Survival (N=856), the Irradiated Group (N=597), the Nonirradiated Group (N=259), and the General U.S. Population Matched for Age, Sex, and Race.). Twenty-one patients, of whom 18 were in the irradiated group, died at 1.0 to 17.6 years (median, 5.5) from base line. Of the 18 deaths in the irradiated group, 12 were due to a second cancer and 1 was due to a relapse of leukemia. Of the three deaths in the nonirradiated group, two were due to suicide and one to a car accident. According to multivariate analysis adjusted for age at the diagnosis of acute lymphoblastic leukemia, sex, race, and treatment era, the probability of survival did not differ significantly between the irradiated and nonirradiated groups (hazard ratio for death in the irradiated group, 1.27; 95 percent confidence interval, 0.36 to 4.47; P=0.71). Comparison of survival data between patients and the general population revealed a higher standardized mortality ratio in the irradiated group (1.90; 95 percent confidence interval, 1.12 to 3.00) but not in the nonirradiated group (1.75; 95 percent confidence interval, 0.34 to 5.00).Marital, Employment, and Health Insurance Status and Access to Health Care
Of the 694 eligible patients, 584 (84.1 percent) responded to the study questionnaire. Only 44 patients (6.3 percent) declined to participate; current addresses and telephone numbers were not available for the remaining 66 patients. The median age of the respondents was 27 years (range, 18 to 50), and the median time from the diagnosis of leukemia to the date of response to the survey was 20 years (range, 10 to 37). Forty-seven percent of the respondents were men.
The marital rate (the proportion of patients currently married) was similar to that in the age- and sex-matched general population, with the exception of women in the irradiated group, whose marital rate (35.2 percent; 95 percent confidence interval, 27.6 to 43.3 percent) was lower than in the corresponding general population (48.8 percent) (Table 4Table 4
Marital, Employment, and Health Insurance Status According to Sex and History of Irradiation.). Most respondents were employed full time (51.7 percent) or part time (7.8 percent); 22.0 percent were students. The rate of full-time employment for nonirradiated patients was similar to that of the age- and sex-matched general population (Table 4). However, in the irradiated group the unemployment rates for both women (35.4 percent; 95 percent confidence interval, 27.0 to 44.1 percent) and men (15.1 percent; 95 percent confidence interval, 9.2 to 22.7 percent) were higher than those in the corresponding general population (5.2 and 5.4 percent, respectively); women in the irradiated group were also less likely to be employed full time.Health insurance was provided through the employer, spouse, or parent in 59.2 percent of cases; federal or state-supported health plans in 15.1 percent; and self-purchase in 6.9 percent. Only 19.7 percent of the respondents lacked health insurance. A history of leukemia had resulted in the denial of health insurance to 28.4 percent of the respondents, prohibitive premiums for 18.6 percent, and restrictions on health care plans for 7.0 percent. As compared with those with private insurance, respondents with public insurance were more likely to report some difficulty in obtaining health care (13.9 percent vs. 6.6 percent) or not receiving needed care (20.9 percent vs. 4 percent). Not surprisingly, an even greater proportion of uninsured survivors reported difficulties in obtaining health care (19.6 percent) or not receiving needed care (27.7 percent). Although 89.3 percent of the long-term survivors reported using a community physician for their health care needs, only 53.2 percent had seen a physician in the preceding 12 months.
Multiple logistic-regression analysis, adjusted for potentially confounding factors, indicated similar rates of health insurance coverage and marriage for irradiated and nonirradiated patients of the same sex. However, the unemployment rate was higher among female survivors in the irradiated group than in the nonirradiated group (odds ratio, 2.15; 95 percent confidence interval, 1.10 to 4.20).
Discussion
Among survivors of childhood acute lymphoblastic leukemia who were event-free for 10 years after the induction of remission, the cumulative risk of relapse was only 0.63±0.32 percent at 20 years (30 years after the induction of an initial complete remission). Another research group reported an actuarial risk of relapse of 1 percent at 20 years of follow-up among 1134 survivors who were event-free for 10 years and who had been treated between 1970 and 1984, but the investigators did not determine the incidence of other adverse events in their cohort.22 The risk of late relapse is likely to be even less in survivors who are event-free for 10 years and who have been treated according to contemporary protocols.23 Our results suggest a new working definition of cure: 10 or more years of continuous complete remission, a standard that could be used to gauge the effectiveness of current and future treatment plans.
The cumulative risk of second neoplasms in children treated for acute lymphoblastic leukemia is less than 4 percent 15 to 20 years after the diagnosis.3,6,24-27 Our study showed that the cumulative incidence of second neoplasms in patients who received cranial or craniospinal irradiation rose sharply 20 years after the diagnosis of acute lymphoblastic leukemia, a finding not previously appreciated because of shorter follow-up in other studies. Most of these late-onset second neoplasms were benign tumors or low-grade cancers, and only 12 of 44 patients with second neoplasms died, in contrast to the high mortality rate among patients whose second neoplasms developed within 10 years after the diagnosis of acute lymphoblastic leukemia.3,6-8,24-29 Consequently, the long-term survival in the irradiated group in our study was only slightly less than that in sex- and age-matched persons in the general population (Figure 3). Survival in the nonirradiated group was virtually identical to that in the general population.
Any assessment of the long-term survival of persons cured of cancer must consider the quality of life.30 Young adult survivors of childhood cancer have lower marital rates than the general population,31-36 and survivors of brain tumors are especially vulnerable.32,36 This finding has been attributed to the sequelae of the treatment, including neuroendocrine dysfunction that affects height and body build and neurocognitive deficits that influence social and emotional development.32 Cranial irradiation is a risk factor for learning deficits in survivors of brain tumors or acute lymphoblastic leukemia, especially in young patients treated with high doses of radiation.35,37
Although the doses of cranial radiation delivered to our patients were relatively low (18 to 24 Gy), we found higher unemployment rates and lower marital rates among the women in the irradiated group than in the age- and sex-matched general population, a result consistent with the greater vulnerability of female patients to the adverse effects of cranial irradiation on the central nervous system.38-40 These results support current efforts to limit the use of cranial irradiation in initial therapy for acute lymphoblastic leukemia.3,41,42 In two recently published clinical trials, cranial irradiation was omitted altogether, without an undue increase in the rate of central nervous system relapse.43,44
Previous investigations of the insurance coverage of survivors of childhood cancer found clear evidence of discrimination, particularly in employment-related health insurance.34,35,45-49 Survivors were also more likely than sibling controls to have policies with clauses excluding coverage of preexisting health conditions.34,35,48 More recent studies of older survivors treated according to contemporary protocols indicate improved access to insurance and less economic discrimination,34,35 probably because of the public's awareness of the favorable prognosis for most survivors of childhood cancer and because of legislation prohibiting discrimination in employment and promoting insurance portability.50-52 Our data indicate that the rate of insurance coverage for long-term survivors of acute lymphoblastic leukemia is at least similar to or, in the case of female survivors, higher than that in the general population.
Adult survivors of childhood cancer are at risk for health problems that may adversely affect their quality of life and long-term survival.7,8,53,54 Because these risks may be exacerbated by the physiologic changes associated with normal aging, lifelong medical monitoring is recommended for all survivors of childhood cancer. Although 89 percent of the survivors of acute lymphoblastic leukemia who were discharged from follow-up at our institution reported having a usual place to obtain health care, only 53 percent had had a medical evaluation within the previous year. This rate appears to be lower than that in the general population (approximately 80 percent),55 underscoring the need for further investigation of the patterns of health care use among long-term survivors of acute lymphoblastic leukemia.
Supported in part by a grant (21765) from the National Institutes of Health, a Center of Excellence grant from the state of Tennessee, and the American Lebanese Syrian Associated Charities. Dr. Pui is the American Cancer Society F.M. Kirby Clinical Research Professor.
We are indebted to Deqing Pei and Shelly Lensing for statistical analysis, Dr. James Boyett for statistical consultation, John Gilbert for assistance with scientific editing, Dr. Sarah Scholle for assistance with the insurance survey, Annette Stone and Margie Zacher for data management, Julie Groff for assistance with the figures, Kimberly Gayden for assistance in the preparation of the manuscript, many physicians (especially Drs. Rhomes J. Aur, H. Omar Hustu, Donald Pinkel, and Joseph V. Simone) for their contributions to the design and conduct of early Total Therapy studies, and the many patients and parents who participated in the research program.
Source Information
From the Departments of Hematology–Oncology (C.-H.P., W.L., G.K.R., J.T.S., R.C.R., M.M.H.), Pathology (C.-H.P.), Biostatistics (C.C., S.N.R.), Pharmaceutical Sciences (M.V.R., W.E.E.), and Radiation Oncology (L.E.K.), St. Jude Children's Research Hospital; and the Colleges of Medicine (C.-H.P., W.L., G.K.R., J.T.S., R.C.R., M.V.R., L.E.K., W.E.E., M.M.H.) and Pharmacy (M.V.R., W.E.E.), University of Tennessee Health Science Center — all in Memphis.
Address reprint requests to Dr. Pui at St. Jude Children's Research Hospital, 332 N. Lauderdale, Memphis, TN 38105, or at ching-hon.pui@stjude.org.
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- Citing Articles (118)
Citing Articles
1
L. B. Travis, A. K. Ng, J. M. Allan, C.-H. Pui, A. R. Kennedy, X. G. Xu, J. A. Purdy, K. Applegate, J. Yahalom, L. S. Constine, E. S. Gilbert, J. D. Boice. (2012) Second Malignant Neoplasms and Cardiovascular Disease Following Radiotherapy. JNCI Journal of the National Cancer Institute
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Graziella Filippini. 2012. Epidemiology of primary central nervous system tumors. , 3-22.
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Trish Scanlan, Jane Kaijage. (2012) From Denis Burkitt to Dar es Salaam. What happened next in East Africa? - Tanzania’s story. British Journal of Haematologyno-no
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Lisa Cancemi, Cristina Romei, Sara Bertocchi, Giulia Tarrini, Irene Spitaleri, Monica Cipollini, Debora Landi, Sonia Garritano, Giovanni Pellegrini, Alfonso Cristaudo, Aldo Pinchera, Roberto Barale, Rossella Elisei, Stefano Landi, Federica Gemignani. (2011) Evidences that the polymorphism Pro-282-Ala within the tumor suppressor gene WWOX is a new risk factor for differentiated thyroid carcinoma. International Journal of Cancer 129:12, 2816-2824
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Susanne Vinkel Koch, Anne Mette Tranberg Kejs, Gerda Engholm, Henrik Møller, Christoffer Johansen, Kjeld Schmiegelow. (2011) Marriage and Divorce Among Childhood Cancer Survivors. Journal of Pediatric Hematology/Oncology 33:7, 500-505
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Joy M. Fulbright, Sripriya Raman, Wendy S. McClellan, Keith J. August. (2011) Late Effects of Childhood Leukemia Therapy. Current Hematologic Malignancy Reports 6:3, 195-205
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William L. Carroll, Elizabeth A. Raetz. (2011) Clinical and Laboratory Biology of Childhood Acute Lymphoblastic Leukemia. The Journal of Pediatrics
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E. Park, E. J. Gang, Y.-T. Hsieh, P. Schaefer, S. Chae, L. Klemm, S. Huantes, M. Loh, E. M. Conway, E.-S. Kang, H. Hoe Koo, W.-K. Hofmann, N. Heisterkamp, L. Pelus, G. Keerthivasan, J. Crispino, M. Kahn, M. Muschen, Y.-M. Kim. (2011) Targeting survivin overcomes drug resistance in acute lymphoblastic leukemia. Blood 118:8, 2191-2199
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Marleen Renard, Stefan Suciu, Yves Bertrand, Anne Uyttebroeck, Alice Ferster, Jutte van der Werff ten Bosch, Françoise Mazingue, Emannuel Plouvier, Alain Robert, Patrick Boutard, Frédéric Millot, Martine Munzer, Françoise Mechinaud, Brigitte Lescoeur, Liliana Baila, Els Vandecruys, Yves Benoit, Pierre Philippet, . (2011) Second neoplasm in children treated in EORTC 58881 trial for acute lymphoblastic malignancies: Low incidence of CNS tumours. Pediatric Blood & Cancer 57:1, 119-125
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J. WANG, W. LI, L. LI, X. YU, J. JIA, C. CHEN. (2011) CIP2A is over-expressed in acute myeloid leukaemia and associated with HL60 cells proliferation and differentiation. International Journal of Laboratory Hematology 33:3, 290-298
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Melissa M. Hudson, Kirsten K. Ness, Vikki G. Nolan, Gregory T. Armstrong, Daniel M. Green, E. Brannon Morris, Sheri L. Spunt, Monika L. Metzger, Kevin R. Krull, James L. Klosky, Deo Kumar Srivastava, Leslie L. Robison. (2011) Prospective medical assessment of adults surviving childhood cancer: Study design, cohort characteristics, and feasibility of the St. Jude Lifetime Cohort Study. Pediatric Blood & Cancer 56:5, 825-836
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C. Oudin, M.-C. Simeoni, N. Sirvent, A. Contet, A. Begu-Le Coroller, P. Bordigoni, C. Curtillet, M. Poiree, I. Thuret, B. Play, M. C. Massot, P. Chastagner, H. Chambost, P. Auquier, G. Michel. (2011) Prevalence and risk factors of the metabolic syndrome in adult survivors of childhood leukemia. Blood 117:17, 4442-4448
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Hui-Ling Cheng, Shyh-Shin Chiou, Yu-Mei Liao, Yen-Ling Chen, Shou-Mei Wu. (2011) Genotyping of two single nucleotide polymorphisms in 5,10-methylenetetrahydrofolate reductase by multiplex polymerase chain reaction and capillary electrophoresis. Journal of Chromatography A 1218:15, 2114-2120
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Judith Frances Margolin. (2011) Molecular diagnosis and risk-adjusted therapy in pediatric hematologic malignancies: a primer for pediatricians. European Journal of Pediatrics 170:4, 419-425
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Manmeet S. Ahluwalia, Paul K. Wallace, David M. Peereboom. (2011) Flow cytometry as a diagnostic tool in lymphomatous or leukemic meningitis. Cancern/a-n/a
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XiaoHu Wang, Ruifeng Liu, KeHu Yang, Bin Ma, Jinhui Tian, Jun Wang, HongTao Luo, XiaoHu Wang. 2010. Treatment including intrathecal chemotherapy with and without cranial irradiation for prevention of central nervous system relapse of childhood acute lymphoblastic leukemia. .
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Shyh-Shin Chiou, Ren-Chin Jang, Yu-Mei Liao, Pinchen Yang. (2010) Health-related quality of life and cognitive outcomes among child and adolescent survivors of leukemia. Supportive Care in Cancer 18:12, 1581-1587
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Dario Campana, Ching-Hon Pui. 2010. Childhood Acute Lymphoblastic Leukaemia. , 448-462.
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James E. Jacobs, Caroline Hastings. (2010) Isolated Extramedullary Relapse in Childhood Acute Lymphocytic Leukemia. Current Hematologic Malignancy Reports 5:4, 185-191
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Deborah Thomas, Susan O'Brien, Stefan Faderl, Farhad Ravandi, Elias Jabbour, Sherry Pierce, Jorge Cortes, Hagop Kantarjian. (2010) Anthracycline dose intensification in adult acute lymphoblastic leukemia. Cancer 116:19, 4580-4589
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Anna Sällfors Holmqvist, Thomas Wiebe, Lars Hjorth, Anna Lindgren, Ingrid Øra, Christian Moëll. (2010) Young age at diagnosis is a risk factor for negative late socio-economic effects after acute lymphoblastic leukemia in childhood. Pediatric Blood & Cancer 55:4, 698-707
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Keisuke Kato, Chie Kobayashi, Kazuko Kudo, Takashi Hara, Kyoko Masuko, Kazutoshi Koike, Masahiro Tsuchida. (2010) Late Recurrence of Precursor B-cell Acute Lymphoblastic Leukemia 9 Years and 7 Months After Allogeneic Hematopoietic Stem Cell Transplantation. Journal of Pediatric Hematology/Oncology 32:7, e290-e293
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Nicole M.E. Bradley, Maria F. Lorenzi, Zenaida Abanto, Sam Sheps, Anne Marie Broemeling, John J. Spinelli, Karen Goddard, Sheila Pritchard, Paul Rogers, Mary L. McBride. (2010) Hospitalisations 1998–2000 in a British Columbia population-based cohort of young cancer survivors: Report of the Childhood/Adolescent/Young Adult Cancer Survivors (CAYACS) Research Program. European Journal of Cancer 46:13, 2441-2448
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Brad J. Zebrack, Sallie Foley, Daniela Wittmann, Marcia Leonard. (2010) Sexual functioning in young adult survivors of childhood cancer. Psycho-Oncology 19:8, 814-822
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Pinki K. Prasad, Travis Bowles, Debra L. Friedman. (2010) Is there a role for a specialized follow-up clinic for survivors of pediatric cancer?. Cancer Treatment Reviews 36:4, 372-376
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Samart Pakakasama, Gavivann Veerakul, Darin Sosothikul, Su-on Chainansamit, Vichai Laosombat, Pattra Thanarattanakorn, Rachata Lumkul, Surapon Wiangnon, Somporn Wangruangsathit, Nattee Narkbunnam, Somjai Kanjanapongkul. (2010) Late effects in survivors of childhood acute lymphoblastic leukemia: a study from Thai Pediatric Oncology Group. International Journal of Hematology 91:5, 850-854
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Wing Leung, Geoffrey Neale, Fred Behm, Rekha Iyengar, David Finkelstein, Michael B. Kastan, Ching-Hon Pui. (2010) Deficient innate immunity, thymopoiesis, and gene expression response to radiation in survivors of childhood acute lymphoblastic leukemia. Cancer Epidemiology 34:3, 303-308
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Vassilios Papadakis, Eleftheria Roma, Kalliopi Stefanaki, Ioanna Panagiotou, Sofia Papargyri, George Paterakis, Sofia Polychronopoulou. (2010) Gastrointestinal presentation of late acute lymphoblastic leukemia relapse. Pediatrics International 52:3, e171-e174
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Shadi Farzin Gohar, Victoria Marchese, Melanie Comito. (2010) PHYSICIAN REFERRAL FREQUENCY FOR PHYSICAL THERAPY IN CHILDREN WITH ACUTE LYMPHOBLASTIC LEUKEMIA. Pediatric Hematology-Oncology 27:3, 179-187
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C H Pui, D Pei, J T Sandlund, R C Ribeiro, J E Rubnitz, S C Raimondi, M Onciu, D Campana, L E Kun, S Jeha, C Cheng, S C Howard, M L Metzger, D Bhojwani, J R Downing, W E Evans, M V Relling. (2010) Long-term results of St Jude Total Therapy Studies 11, 12, 13A, 13B, and 14 for childhood acute lymphoblastic leukemia. Leukemia 24:2, 371-382
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Melissa M Hudson. (2010) Pediatric cancer survivorship: is our work nearly done or just beginning?. Pediatric Health 4:1, 5-7
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D-C Liang, C-P Yang, D-T Lin, I-J Hung, K-H Lin, J-S Chen, C-C Hsiao, T-T Chang, C-T Peng, M-T Lin, T-K Chang, T-H Jaing, H-C Liu, L-Y Wang, T-C Yeh, S-T Jou, M-Y Lu, C-N Cheng, J-M Sheen, S-S Chiou, K-H Wu, G-Y Hung, R-L Chen, S-H Chen, S-N Cheng, Y-H Chang, B-W Chen, W-L Ho, J-L Wang, S-T Lin, Y-L Hsieh, S-C Wang, H-H Chang, Y-L Yang, F-L Huang, C-Y Chang, W-H Chang, K-S Lin. (2010) Long-term results of Taiwan Pediatric Oncology Group studies 1997 and 2002 for childhood acute lymphoblastic leukemia. Leukemia 24:2, 397-405
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George A. Alexiou, Maria Moschovi, George Georgoulis, Rosalia Neroutsou, Kalliopi Stefanaki, George Sfakianos, Neofytos Prodromou. (2010) Anaplastic oligodendrogliomas after treatment of acute lymphoblastic leukemia in children. Journal of Neurosurgery: Pediatrics 5:2, 179-183
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Ram K. Marwaha, Ketan P. Kulkarni, Deepak Bansal, Amita Trehan. (2010) Central nervous system involvement at presentation in childhood acute lymphoblastic leukemia: management experience and lessons. Leukemia & Lymphoma 51:2, 261-268
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Francesca Giusti, Alberto Falchetti, Francesco Franceschelli, Francesca Marini, Annalisa Tanini, Maria Luisa Brandi. (2010) Thyroid Cancer: Current Molecular Perspectives. Journal of Oncology 2010, 1-17
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Clare Frobisher, Emma R. Lancashire, David L. Winter, Aliki J. Taylor, Raoul C. Reulen, Michael M. Hawkins, . (2010) Long-term population-based divorce rates among adult survivors of childhood cancer in Britain. Pediatric Blood & Cancer 54:1, 116-122
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Elias Jabbour, Deborah Thomas, Jorge Cortes, Hagop M. Kantarjian, Susan O'Brien. (2010) Central nervous system prophylaxis in adults with acute lymphoblastic leukemia. CancerNA-NA
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D Pinkel. (2009) ‘Allogeneic marrow transplantation in children with acute leukemia: a practice whose time has gone’: twenty years later. Leukemia 23:12, 2189-2196
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Sima Jeha, Ching-Hon Pui. (2009) Risk-adapted Treatment of Pediatric Acute Lymphoblastic Leukemia. Hematology/Oncology Clinics of North America 23:5, 973-990
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(2009) Treating Childhood Leukemia without Cranial Irradiation. New England Journal of Medicine 361:13, 1310-1312
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Ching-Hon Pui, Eckhard Thiel. (2009) Central Nervous System Disease in Hematologic Malignancies: Historical Perspective and Practical Applications. Seminars in Oncology 36, S2-S16
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H. MAURICE-STAM, F.J. OORT, B.F. LAST, M.A. GROOTENHUIS. (2009) A predictive model of health-related quality of life in young adult survivors of childhood cancer. European Journal of Cancer Care 18:4, 339-349
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Amber Fullmer, Susan O’Brien, Hagop Kantarjian, Elias Jabbour. (2009) Novel therapies for relapsed acute lymphoblastic leukemia. Current Hematologic Malignancy Reports 4:3, 148-156
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Pui, Ching-Hon, Campana, Dario, Pei, Deqing, Bowman, W. Paul, Sandlund, John T., Kaste, Sue C., Ribeiro, Raul C., Rubnitz, Jeffrey E., Raimondi, Susana C., Onciu, Mihaela, Coustan-Smith, Elaine, Kun, Larry E., Jeha, Sima, Cheng, Cheng, Howard, Scott C., Simmons, Vickey, Bayles, Amy, Metzger, Monika L., Boyett, James M., Leung, Wing, Handgretinger, Rupert, Downing, James R., Evans, William E., Relling, Mary V., . (2009) Treating Childhood Acute Lymphoblastic Leukemia without Cranial Irradiation. New England Journal of Medicine 360:26, 2730-2741
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T. J. Achterberg, H. Wind, A. G. E. M. Boer, M. H. W. Frings-Dresen. (2009) Factors that Promote or Hinder Young Disabled People in Work Participation: A Systematic Review. Journal of Occupational Rehabilitation 19:2, 129-141
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Patrick Brown, Steven P Hunger, Franklin O Smith, William L Carroll, Gregory H Reaman. (2009) Novel targeted drug therapies for the treatment of childhood acute leukemia. Expert Review of Hematology 2:2, 145-158
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Sima Jeha. (2009) New Therapeutic Strategies in Acute Lymphoblastic Leukemia. Seminars in Hematology 46:1, 76-88
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Po-Ching Chu, Jung-Der Wang, Jing-Shiang Hwang, Yu-Yin Chang. (2008) Estimation of Life Expectancy and the Expected Years of Life Lost in Patients with Major Cancers: Extrapolation of Survival Curves under High-Censored Rates. Value in Health 11:7, 1102-1109
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Evguenia J. Karimova, Shesh N. Rai, Jianrong Wu, Lunetha Britton, Sue C. Kaste, Michael D. Neel. (2008) Femoral Resurfacing in Young Patients with Hematologic Cancer and Osteonecrosis. Clinical Orthopaedics and Related Research 466:12, 3044-3050
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Aneta Pobudejska, Danuta Sońta-Jakimczyk, Marta Pawełczak-Szastok. (2008) Ocena stanu zdrowia i jakości życia osób leczonych w dzieciństwie z powodu ostrej białaczki limfoblastycznej. Pediatria Polska 83:6, 656-661
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J. D. Rizzo, R. E. Curtis, G. Socie, K. A. Sobocinski, E. Gilbert, O. Landgren, L. B. Travis, W. D. Travis, M. E. D. Flowers, D. L. Friedman, M. M. Horowitz, J. R. Wingard, H. J. Deeg. (2008) Solid cancers after allogeneic hematopoietic cell transplantation. Blood 113:5, 1175-1183
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Astri Syse. (2008) Does cancer affect marriage rates?. Journal of Cancer Survivorship 2:3, 205-214
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A Shah, C A Stiller, M G Kenward, T Vincent, T O B Eden, M P Coleman. (2008) Childhood leukaemia: long-term excess mortality and the proportion ‘cured’. British Journal of Cancer 99:1, 219-223
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R. Mody, S. Li, D. C. Dover, S. Sallan, W. Leisenring, K. C. Oeffinger, Y. Yasui, L. L. Robison, J. P. Neglia. (2008) Twenty-five-year follow-up among survivors of childhood acute lymphoblastic leukemia: a report from the Childhood Cancer Survivor Study. Blood 111:12, 5515-5523
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Maureen M. O’Brien, Normal J. Lacayo. (2008) Acute Leukemia in Children. Disease-a-Month 54:4, 202-225
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Ching-Hon Pui, Leslie L Robison, A Thomas Look. (2008) Acute lymphoblastic leukaemia. The Lancet 371:9617, 1030-1043
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Wei-Ying Lin, Hsi-Che Liu, Ting-Chi Yeh, Lin-Yen Wang, Der-Cherng Liang. (2008) Triple intrathecal therapy without cranial irradiation for central nervous system preventive therapy in childhood acute lymphoblastic leukemia. Pediatric Blood & Cancer 50:3, 523-527
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Ching-Hon Pui, Scott C Howard. (2008) Current management and challenges of malignant disease in the CNS in paediatric leukaemia. The Lancet Oncology 9:3, 257-268
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Roberto Bernaldez-Rios, Manuel C. Ortega-Alvarez, Maria L. Perez-Saldivar, Norma E. Alatoma-Medina, Maria de los A. Del Campo-Martinez, Maria del Carmen Rodriguez-Zepeda, Ines Montero-Ponce, Sergio Franco-Ornelas, Gabriela Fernandez-Castillo, Nora N. Nuñez-Villegas, Miguel A. Taboada-Flores, Janet Flores-Lujano, Muriel E. Argüelles-Sanchez, Servando Juarez-Ocaña, Arturo Fajardo-Gutierrez, Juan Manuel Mejia-Arangure. (2008) The Age Incidence of Childhood B-cell Precursor Acute Lymphoblastic Leukemia in Mexico City. Journal of Pediatric Hematology/Oncology 30:3, 199-203
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Firoz Ahmad, Rupa Dalvi, Deepak Chavan, Bibhu Ranjan Das, Swarna Mandava. (2008) Cytogenetic profile of acute lymphocytic leukemia patients: report of a novel translocation t(4;13) (q21·3; q35) from an Indian population. Hematology 13:1, 28-33
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Daniel A. Mulrooney, Joseph P. Neglia, Melissa M. Hudson. (2008) Caring for Adult Survivors of Childhood Cancer. Current Treatment Options in Oncology 9:1, 51-66
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M Eapen, M-J Zhang, M Devidas, E Raetz, J C Barredo, A K Ritchey, K Godder, S Grupp, V A Lewis, K Malloy, W L Carroll, S M Davies, B M Camitta. (2008) Outcomes after HLA-matched sibling transplantation or chemotherapy in children with acute lymphoblastic leukemia in a second remission after an isolated central nervous system relapse: a collaborative study of the Children's Oncology Group and the Center for International Blood and Marrow Transplant Research. Leukemia 22:2, 281-286
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Laura A. Janzen, Brenda J. Spiegler. (2008) Neurodevelopmental sequelae of pediatric acute lymphoblastic leukemia and its treatment. Developmental Disabilities Research Reviews 14:3, 185-195
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Jenny W.Y. Pang, Debra L. Friedman, John A. Whitton, Marilyn Stovall, Ann C. Mertens, Leslie L. Robison, Noel S. Weiss. (2008) Employment status among adult survivors in the Childhood Cancer Survivor Study. Pediatric Blood & Cancer 50:1, 104-110
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M. V. Relling, W. E. Evans, C.-H. Pui. (2008) Continue to study childhood ALL. Blood 111:1, 468-469
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G. Michel. (2008) Leucemia linfobl??stica aguda del ni??o y del adolescente: cl??nica y tratamiento. EMC - Pediatr??a 43:4, 1-11
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Raul Ribeiro, Ching-Hon Pui. (2008) Treatment of acute lymphoblastic leukemia in low- and middle-income countries: Challenges and opportunities. Leukemia & Lymphoma 49:3, 373-376
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Anja Borgmann, Christina Zinn, Reinhard Hartmann, Ralf Herold, Peter Kaatsch, Gabriele Escherich, Anja Möricke, Günter Henze, Arend von Stackelberg. (2008) Secondary malignant neoplasms after intensive treatment of relapsed acute lymphoblastic leukaemia in childhood. European Journal of Cancer 44:2, 257-268
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Cynthia A. Gerhardt, Meredith Dixon, Kimberly Miller, Kathyrn Vannatta, Kristin S. Valerius, Judy Correll, Robert B. Noll. (2007) Educational and Occupational Outcomes Among Survivors of Childhood Cancer During the Transition to Emerging Adulthood. Journal of Developmental & Behavioral Pediatrics 28:6, 448-455
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Brian Knab, Philip P Connell. (2007) Radiotherapy for pediatric brain tumors: when and how. Expert Review of Anticancer Therapy 7:12s, S69-S77
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G Michel, P Bordigoni, M-C Simeoni, C Curtillet, S Hoxha, S Robitail, I Thuret, S Pall-Kondolff, H Chambost, D Orbicini, P Auquier. (2007) Health status and quality of life in long-term survivors of childhood leukaemia: the impact of haematopoietic stem cell transplantation. Bone Marrow Transplantation 40:9, 897-904
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Y LEE, S SANTACROCE. (2007) Posttraumatic stress in long-term young adult survivors of childhood cancer: A questionnaire survey. International Journal of Nursing Studies 44:8, 1406-1417
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Fred H. Laningham, Larry E. Kun, Wilburn E. Reddick, Robert J. Ogg, E. Brannon Morris, Ching-Hon Pui. (2007) Childhood central nervous system leukemia: historical perspectives, current therapy, and acute neurological sequelae. Neuroradiology 49:11, 873-888
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Deborah B. Crom, Shelly Y. Lensing, Shesh N. Rai, Mark A. Snider, Darlene K. Cash, Melissa M. Hudson. (2007) Marriage, employment, and health insurance in adult survivors of childhood cancer. Journal of Cancer Survivorship 1:3, 237-245
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Yacov Goshen, Batia Stark, Liora Kornreich, Shalom Michowiz, Meora Feinmesser, Isaac Yaniv. (2007) High incidence of meningioma in cranial irradiated survivors of childhood acute lymphoblastic leukemia. Pediatric Blood & Cancer 49:3, 294-297
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A. R. Chauvenet, P. L. Martin, M. Devidas, S. B. Linda, B. A. Bell, J. Kurtzberg, J. Pullen, M. J. Pettenati, A. J. Carroll, J. J. Shuster, B. Camitta. (2007) Antimetabolite therapy for lesser-risk B-lineage acute lymphoblastic leukemia of childhood: a report from Children's Oncology Group Study P9201. Blood 110:4, 1105-1111
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Wing Leung, Hyunah Ahn, Susan R. Rose, Sean Phipps, Teresa Smith, Kwan Gan, Madeline O'Connor, Gregory A. Hale, Kimberly A. Kasow, Raymond C. Barfield, Renee M. Madden, Ching-Hon Pui. (2007) A Prospective Cohort Study of Late Sequelae of Pediatric Allogeneic Hematopoietic Stem Cell Transplantation. Medicine 86:4, 215-224
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Marc Ansari, Maja Krajinovic. (2007) Pharmacogenomics of acute leukemia. Pharmacogenomics 8:7, 817-834
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Hind Medyouf, Hélène Alcalde, Caroline Berthier, Marie Claude Guillemin, Nuno R dos Santos, Anne Janin, Didier Decaudin, Hugues de Thé, Jacques Ghysdael. (2007) Targeting calcineurin activation as a therapeutic strategy for T-cell acute lymphoblastic leukemia. Nature Medicine 13:6, 736-741
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M. Maule, G. Scelo, G. Pastore, P. Brennan, K. Hemminki, E. Tracey, R. Sankila, E. Weiderpass, J. H. Olsen, M. L. McBride, D. H. Brewster, V. Pompe-Kirn, E. V. Kliewer, K. S. Chia, J. M. Tonita, C. Martos, J. G. Jonasson, F. Merletti, P. Boffetta. (2007) Risk of Second Malignant Neoplasms After Childhood Leukemia and Lymphoma: An International Study. JNCI Journal of the National Cancer Institute 99:10, 790-800
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Masoud Solaymani-Dodaran, Joe West, Richard F.A. Logan. (2007) Long-Term Mortality in People With Celiac Disease Diagnosed in Childhood Compared With Adulthood: A Population-Based Cohort Study. The American Journal of Gastroenterology 102:4, 864-870
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Akira Kikuchi, Miho Maeda, Ryoji Hanada, Yuri Okimoto, Koichi Ishimoto, Takashi Kaneko, Koichiro Ikuta, Masahiro Tsuchida, . (2007) Moyamoya syndrome following childhood acute lymphoblastic leukemia. Pediatric Blood & Cancer 48:3, 268-272
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Ching-Hon Pui, Sima Jeha. (2007) New therapeutic strategies for the treatment of acute lymphoblastic leukaemia. Nature Reviews Drug Discovery 6:2, 149-165
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Bernd F. M. Romeike, Yoo-Jin Kim, Wolf-Ingo Steudel, Norbert Graf. (2007) Diffuse high-grade gliomas as second malignant neoplasms after radio-chemotherapy for pediatric malignancies. Child's Nervous System 23:2, 185-193
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Michael Weintraub, Eitan Gross, Avishag Kadari, Vardit Ravitsky, Anat Safran, Neri Laufer, Ariel Revel. (2007) Should ovarian cryopreservation be offered to girls with cancer. Pediatric Blood & Cancer 48:1, 4-9
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R. Menon, D. Muzumdar, A. Shah, A. Goel. (2007) Glioblastoma Multiforme following Cranial Irradiation and Chemotherapy for Acute Lymphocytic Leukaemia. Pediatric Neurosurgery 43:5, 369-374
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Quentin A. Hill, Roger G. Owen. (2006) CNS prophylaxis in lymphoma: Who to target and what therapy to use. Blood Reviews 20:6, 319-332
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Melissa M. Hudson, Sheri Findlay. (2006) Health-risk behaviors and health promotion in adolescent and young adult cancer survivors. Cancer 107:S7, 1695-1701
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Lori Wiener, Haven Battles, Donna Bernstein, Lauren Long, Joanne Derdak, Crystal L. Mackall, Patrick J. Mansky. (2006) Persistent psychological distress in long-term survivors of pediatric sarcoma: the experience at a single institution. Psycho-Oncology 15:10, 898-910
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Ginger E Holt, A Brian Thomson, A M Griffin, R Bell, J Wunder, Bruce Rougraff, Herbert S Schwartz. (2006) Multifocality and Multifocal Postradiation Sarcomas. Clinical Orthopaedics and Related Research 450, 67-75
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Anna G.E.M. de Boer, Jozef H.A.M. Verbeek, Franciscus J.H. van Dijk. (2006) Adult survivors of childhood cancer and unemployment. Cancer 107:1, 1-11
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Susanne Vinkel Koch, Anne Mette Tranberg Kejs, Gerda Engholm, Henrik Møller, Christoffer Johansen, Kjeld Schmiegelow. (2006) Leaving home after cancer in childhood: A measure of social independence in early adulthood. Pediatric Blood & Cancer 47:1, 61-70
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Joseph V. Simone. (2006) History of the treatment of childhood ALL: A paradigm for cancer cure. Best Practice & Research Clinical Haematology 19:2, 353-359
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J. F. Cornelius, B. George, F. Kolb. (2006) Combined use of a radial fore arm free flap for extra-intracranial bypass and for antero-lateral skull base reconstruction – a new technique and review of literature. Acta Neurochirurgica 148:4, 427-434
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Catharyn J. STERN, Manuela G. TOLEDO, Debra A. GOOK, John F. SEYMOUR. (2006) Fertility preservation in female oncology patients. The Australian and New Zealand Journal of Obstetrics and Gynaecology 46:1, 15-23
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Debra L. Friedman, David R. Freyer, Gill A. Levitt. (2006) Models of care for survivors of childhood cancer. Pediatric Blood & Cancer 46:2, 159-168
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Kevin C. Oeffinger, W. Hamish B. Wallace. (2006) Barriers to follow-up care of survivors in the United States and the United Kingdom. Pediatric Blood & Cancer 46:2, 135-142
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Pui, Ching-Hon, Evans, William E., . (2006) Treatment of Acute Lymphoblastic Leukemia. New England Journal of Medicine 354:2, 166-178
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Robert E Goldsby, Denah R Taggart, Arthur R Ablin. (2006) Surviving Childhood Cancer. Pediatric Drugs 8:2, 71-84
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H. Stam, M. A. Grootenhuis, H. N. Caron, B. F. Last. (2006) Quality of life and current coping in young adult survivors of childhood cancer: positive expectations about the further course of the disease were correlated with better quality of life. Psycho-Oncology 15:1, 31-43
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Paul C. Nathan, Trish Whitcomb, Pamela L. Wolters, Seth M. Steinberg, Frank M. Balis, Pim Brouwers, Sally Hunsberger, James Feusner, Harland Sather, James Miser, Lorrie F. Odom, David Poplack, Gregory Reaman, W. Archie Bleyer. (2006) Very high-dose methotrexate (33.6 g/m 2 ) as central nervous system preventive therapy for childhood acute lymphoblastic leukemia: results of National Cancer Institute/Children's Cancer Group trials CCG-191P, CCG-134P and CCG-144P. Leukemia & Lymphoma 47:12, 2488-2504
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Murat Sonmezer, Mousa Issa Shamonki, Kutluk Oktay. (2005) Ovarian tissue cryopreservation: benefits and risks. Cell and Tissue Research 322:1, 125-132
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Donna M. Hammal, Claire L. Bell, Alan W. Craft, Louise Parker. (2005) Second primary tumors in children and young adults in the North of England (1968-99). Pediatric Blood & Cancer 45:2, 155-161
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