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Journal of Clinical Oncology, Vol 24, No 16 (June 1), 2006: pp. 2536-2543 © 2006 American Society of Clinical Oncology. DOI: 10.1200/JCO.2005.03.9628 Health-Related Quality of Life Among Child and Adolescent Survivors of Childhood Cancer
From the Departments of Pediatrics and Epidemiology and Biostatistics, University of Western Ontario and Children's Health Research Institute, London; Department of Psychology, Population Health Science Research Institute, Hospital for Sick Children and University of Toronto, Toronto; Centre for Chronic Disease Prevention and Control, Public Health Agency of Canada, Ottawa; Department of Social and Preventive Medicine, Université Laval, Laval, Canada Address reprint requests to K.N. Speechley, PhD, Pediatrics, Children's Hospital of Western Ontario, Westminster Tower E6-203, 800 Commissioners Rd E, London, ON Canada N6C 2V5; e-mail: kathy.speechley{at}lhsc.on.ca
PURPOSE: The main objective was to compare parent-reported health-related quality of life (HRQL) of child and adolescent survivors of childhood cancer to that of controls who had no history of cancer. METHODS: We assessed HRQL of 800 child and adolescent survivors younger than 16 years and 923 randomly selected, age- and sex-matched controls from the general population in a national multicenter retrospective cohort study using the Child Health Questionnaire parent report. Participation was 69% among survivors and 57% among controls. RESULTS: Survivors had means that were consistently lower than controls on the HRQL physical summary (PH; 49.9 v 55.3; P <.005), psychosocial summary (PS; 49.4 v 52.6; P < .005), and all but one of the eight subscale scores. Clinically important survivor-control differences in means on PH were found for survivors of CNS tumors, bone tumors, lymphoma, leukemia, soft tissue sarcoma and Wilms' tumor (differences: –8.7, –7.0, –6.3, –5.4, –4.4, –3.8/100, respectively); on PS, survivors of CNS tumors were most compromised (–6.1/100). Survivor-control differences in both PH and PS were also large for survivors treated with radiation only (–5.8 and –11.9/100, respectively), or radiation combined with surgery (–6.6 and –5.9/100, respectively), or radiation combined with both surgery and chemotherapy (–7.8 and –5.1/100, respectively). Cranial radiation was associated with the most compromised HRQL. CONCLUSION: According to parents, HRQL for survivors was somewhat poorer, overall, than for controls. Survivors of CNS tumors, lymphoma, and leukemia and those patients treated with cranial radiation were reported to have poorest HRQL. These findings support development of guidelines for levels of follow-up care for particular groups of survivors.
Nearly 1,300 children and adolescents are diagnosed with cancer each year in Canada.1 Survival for childhood cancer patients has risen dramatically in the past 30 years due to the incorporation of aggressive multimodal therapies into treatment. Today, more than 75% of children diagnosed with cancer will survive 5 or more years after diagnosis.2-7 As of 2003, about one in every 640 young adults in the United States was a survivor of childhood cancer.5 Consequently, the quality of that survival is obviously of concern.2,8-12 However, little has been published on the effects for long-term survivors as measured by health-related quality of life (HRQL), a multidimensional construct including general health, and physical, emotional, and social functioning. To date, studies of HRQL for childhood cancer survivors have tended to focus on adult survivors only or on samples combining adult and child survivors, the studies have small samples, and include only one type of cancer or a combination of many types of cancer together; and have either no control group or use sibling controls.13-21 Thus, it is difficult to make definitive statements regarding the HRQL of survivors of particular types of childhood cancer, and compare them with survivors of other types of cancer or with their general population counterparts who have not experienced cancer, and especially regarding survivors who have not yet reached adulthood. The primary objective of this article is to compare HRQL, as perceived by parents, in child and adolescent survivors of childhood cancer with that of similarly aged individuals from the general population with no history of cancer. A secondary objective is to determine whether there are particular "at risk" survivors to whom special follow-up strategies might be targeted.
Data came from the Late Effects Study of the Canadian Childhood Cancer Surveillance and Control Program (CCCSCP).22 A detailed description of the study design, methods, and participants is published elsewhere.23 Briefly, survivors of childhood cancer were identified and randomly selected in each of 12 pediatric oncology centers and provincial cancer registries, covering all 10 Canadian provinces. Inclusion criteria were patient diagnosis with a first malignancy between the years 1981 and 1990, survival for at least 5 years after diagnosis, and for this report, patient age younger than 16 years old at study accrual. General population controls with no history of cancer were randomly selected in each province from provincial health insurance records or through random-digit dialing. Frequency matching was used to create a control group with similar age and sex distributions as the survivors. Data were collected between January 1997 and February 2000 using a parent-report mailed questionnaire. Study participants, identified through pediatric oncology centers, cancer registries, or health insurance records, were sent a letter about the study and were telephoned to discuss participation within two weeks of identification. General population controls recruited by random-digit dialing were first contacted by telephone. Participants who agreed to take part in the study were mailed a questionnaire and a consent form that was to be completed and returned using the self-addressed envelope provided. The research ethics board at each participating pediatric oncology center and provincial health insurance agency of each province approved the study protocol. Of 1,162 parents and caregivers of eligible survivors, 800 participated in the study. Of 1,633 parents/caregivers of eligible controls, 923 participated. This resulted in response rates of 69% for survivors and 57% for controls. Participants' HRQL was assessed using the Child Health Questionnaire (CHQ) 50-item parent-report version (CHQ-PF50).24 The CHQ is a generic validated measure.25,26 The results presented in this article are for the eight multi-item CHQ subscale scores focusing on the child's general behavior, mental health, self-esteem, bodily pain, general health, role limitations–emotional, role limitations–physical, and physical functioning, and for two summary scores (physical and psychosocial). Items within each scale were constructed and scored using Likert's method of summated ratings.27 Raw scores representing perception of health status during the past 4 weeks were converted to a 0 to 100 continuum, with a higher score indicating better functioning. Although obtaining self-report of HRQL in addition to parent-report would have been preferable, both practical and ethical concerns dictated the use of the parent-report. Participants' physical health problems were evaluated with questions from the Childhood Cancer Survivor Study.28 The number of stressful life events experienced in the past year was assessed using the Children's Life Stress Scale.29 Parent respondents' mental health was measured using the 5-item Mental Health Index from the Short Form 36 (SF-36) health survey (Medical Outcomes Trust, Waltham, MA),30 in which a higher score indicated better mental health. Information on several family characteristics that could affect HRQL such as ethnicity, parents' education, parents' marital status, parents' employment, and household income was also collected. Survivors' clinical information was extracted from medical charts. Type of cancer was classified according to the International Classification of Childhood Cancer.31 A treatment series included chemotherapy, radiation, and/or surgery. Radiation was stratified by site (cranial v other), and chemotherapy by alkylating agents versus other, given prior evidence of late effects associated with these specific exposures.11 More than one treatment series occurred when the initial planned treatment was extended due to incomplete response or when a new treatment series was initiated after the survivor had relapsed.
Statistical Methods
Effect sizes for all survivor-control differences were calculated to aid in assessing clinical significance. Effect size is the difference in adjusted mean scores between survivors and controls, divided by the unadjusted standard deviation of this difference.32 A common convention is to consider an effect size of 0.20 to 0.49 as "small", 0.5 to 0.79 as "medium", and 0.8 or higher as "large."33 An effect size of 0.5 corresponds to a minimum perceptible difference and thus can be considered a clinically important difference.34
Participant Characteristics Overall, survivors and controls were comparable sociodemographically. A slightly larger proportion of survivors were male and older at study accrual (Table 1). A substantially larger proportion of survivors had multiple physical health problems. Of the respondents, more than 90% were the participants' biological parents and approximately 85% were white (data not shown). Parents of survivors reported a slightly lower level of education than parents of controls, and a slightly smaller number of the parents of survivors were in the highest income category compared with parents of controls. More parents of survivors reported poorer mental health scores also compared with parents of controls. Leukemia and CNS tumors were the two most common diagnoses among survivors (Table 2). The average survivor was 2.2 years old at diagnosis (range, 0 to 9 years with 77% diagnosed before age 4 years) and 9.5 years after diagnosis (range, 6 to 16 years). Most survivors received chemotherapy alone (19%), chemotherapy and surgery (24%), chemotherapy combined with surgery and radiation therapy (19%), or chemotherapy combined with radiation therapy (15%). Fewer survivors received surgery alone (15%), or surgery with radiation therapy only (6%). The vast majority of survivors (87%) experienced only one treatment series.
Global Differences Between Survivors and Controls The mean summary scores for both physical and psychosocial health were significantly lower for survivors than for controls (Table 3). Although the difference in psychosocial summary scores indicated only a small effect (effect size [ES] = 0.25), the physical health and functioning of survivors compared with controls had a clinically significant medium effect (ES = 0.62). Similarly, with the exception of bodily pain, all crude mean subscale scores for HRQL were significantly lower for survivors than for controls. Survivors' mean scores remained significantly lower than those of controls, except for bodily pain after adjustment for confounders, although differences were slightly reduced. The effect size resulting from comparing survivors' and controls' general health was large (ES = 1.39), indicating that parents of survivors rate their children's general health as being much more compromised than parents of controls. Effect sizes for survivor-control differences for the other subscale scores were generally negligible or small, ranging from 0.01 to 0.35.
Effects of Type of Cancer The mean HRQL physical summary scores were significantly lower for survivors of CNS tumors, lymphoma, leukemia, sarcoma, and Wilms' tumor (Table 4). Seven survivor diagnostic groups had considerably worse mean physical summary scores compared with controls with large-to-medium effect sizes: CNS tumors (ES = 1.17); bone tumors (ES = 1.12); lymphoma (ES = 0.95); leukemia (ES = 0.76); soft tissue sarcoma (ES = 0.68); liver tumor (ES = 0.62); and Wilms' tumor (ES = 0.60); which can all be considered clinically significant (Table 4). For psychosocial health, mean scores for survivors of CNS tumors, neuroblastoma, and leukemia were significantly lower than for the control group. The differences of the CNS and bone tumor subgroups compared with controls were large enough to be considered clinically relevant (ES = 0.82 and ES = 1.08, respectively).
Effects of Treatment When survivors were stratified by general types of treatment received (Table 4), the adjusted survivor-control differences in mean physical summary scores were largest among survivors treated with a combination of radiation, surgery, and chemotherapy (–7.8/100); followed by those survivors treated with radiation and surgery (–6.6/100), and radiation only (–5.8/100). The effect sizes for these three treatment groups were large (ES = 1.07, ES = 1.01, and ES = 0.94, respectively), whereas the effect sizes for other treatment combinations were small to medium. For psychosocial health, the largest mean score differences between survivors and controls were for survivors treated with radiation therapy only (–11.9/100), followed by those who had received radiation and surgery (–5.9/100). These differences resulted in clinically relevant effect sizes of 1.59 and 0.78, respectively, whereas the remaining treatment combinations demonstrated small effect sizes. When radiation treatment was stratified by site, survivors exposed to cranial radiation therapy (CRT) had the largest deficits in HRQL summary scores versus controls (Table 4). The two largest effect sizes were for the physical summary scores in survivors treated with a combination of chemotherapy, surgery, and CRT (ES = 1.64) and for the psychosocial summary scores of survivors treated with CRT only (ES = 1.69). Type of chemotherapy (alkylating agents v other) was not differentially associated with HRQL. Nearly all survivors who had received CRT alone or CRT combined with surgery had been diagnosed with a CNS tumor (80% and 94%, respectively), whereas 90% of survivors who had received CRT combined with chemotherapy and surgery were survivors of leukemia (50%) or CNS tumors (40%). Interestingly, although our sample size was extremely small, we did notice that 85% of bone tumor survivors had received alkylating chemotherapy with surgery and/or radiation therapy during treatment. Also, 40% of lymphoma survivors, 57% of soft tissue sarcoma survivors, 60% of neuroblastoma survivors, and 85% of liver tumor survivors had received alkylating chemotherapy alone or combined with surgery and/or radiation therapy. A clinically meaningful survivor-control difference was observed for the physical domain of HRQL when survivors were examined by number of treatment series (Table 4). Effect size moved from medium to large for survivors who had at least two treatment series. None of the other demographic or clinical factors contributed to the survivor-control differences in HRQL.
Effects of Sex and Age When assessed separately by sex, the adjusted survivor-control difference in the mean HRQL physical summary score was slightly larger among girls than boys (girls: –6.1/100; 99.5% CI, –5.8 to –2.6; boys: –4.2/100; 99.5% CI, –7.9 to –4.3), as was the effect size (ES for girls, 0.7; ES for boys, 0.5). No effect for sex was found for differences in psychosocial summary scores. When the individual domains of HRQL were examined by sex, the adjusted survivor-control differences indicated only minimal variations by sex. For girls, there were clinically significant differences for General Health and Physical Functioning. For boys, the only clinically significant difference was for General Health.
Overall, long-term survivors of childhood cancer (> 5 years after diagnosis; most survivors were diagnosed before age 4 years) were reported by their parents to have consistently poorer HRQL than population controls of the same age and sex. The differences in physical health are likely to be clinically relevant. Psychosocial differences were smaller and not likely to be clinically relevant. The general health subscale was the one individual subscale to show clinically significant deficits when compared with controls, suggesting that several years after treatment survivors' parents still see their child's general health as substantially poorer than do parents of children who have not had cancer and tend to worry more about their child's future health. To our knowledge, only two other studies have reported on HRQL in survivors of childhood cancer, who were diagnosed in early childhood and were still children when studied, using a single validated instrument with which we could compare our findings. Shankar et al35 recently found that 90 "off-therapy" survivors, aged 4 to 12 years, self-reported a superior overall quality of life relative to 481 age-matched healthy controls, but the authors suggest that the clinical significance of the size of difference found remains undefined. Shankar et al's results were based on child self-report, whereas our results are based on parent-report. Other differences may also explain the discrepancies between their findings and ours, namely, a relatively small nonrandom sample of survivors with one of only four primary diagnoses and different interview methods for survivors and controls (survivors, in-person; controls, over telephone). Barr et al36 found that parents' reports of HRQL in survivors of Wilms' tumor was comparable with results reported previously in survivors of standard-risk acute lymphoblastic leukemia and with results reported previously in children from the general population, whereas survivors of advanced neuroblastoma had poorer HRQL, a finding similar to that reported in a previous sample of high-risk acute lymphoblastic leukemia patients. These findings, however, are based on small subsamples compared across studies, and the neuroblastoma patients all had advanced-stage disease. Our findings are similar to those reported using the CHQ among a group of children with cancer who had recently completed treatment.37 Close examination of survivors by diagnostic groups did reveal some notable variations in parents' reports of the survivors' HRQL. For the physical domain of HRQL, those patients surviving CNS tumors, lymphoma, leukemia, soft tissue sarcoma, and Wilms' tumor (in descending order) were compromised to an extent considered clinically important. Given the age of the patients in our sample, it was surprising that the neuroblastoma subgroup did not differ significantly from controls. We suspect that these neuroblastoma survivors did not have advanced-stage disease. For the psychosocial domain, survivors of CNS tumors were the only diagnostic group with appreciable negative effects compared with controls. This finding is consistent with recent reports indicating that survivors of CNS tumors not only have greater neurocognitive and attentional deficits than survivors of other childhood cancers,38-41 but are also more psychosocially compromised42-45 and demonstrate lower functional ability than other survivors.19,46 Bone tumor survivors also showed large deficits in both physical and psychosocial components of HRQL, but due to the small sample size we cannot make conclusive statements about this subgroup. Similar to and largely determined by the differences observed by cancer diagnosis, type of treatment received was also associated with survivors' HRQL. Large deficits in both the physical and psychosocial domains were reported for survivors who received radiation therapy, both alone and in combination with surgery, or in combination with surgery and chemotherapy together. Cranial radiation, in particular, contributed the most to the large deficits in HRQL, which is consistent with neurocognitive late effects documented previously47,48; the effect of radiation to other sites resulted in only modest deficits in HRQL. There are some methodologic limitations in this study. The modest response rates raise the possibility of selection bias. Concern regarding possible bias was mitigated by several observations, however. Clinical characteristics of survivors who participated and those who refused to participate or were lost to follow-up were generally comparable.23 The population controls had similar age, sex, ethnic origin, and area of residence distributions as the survivors. The population controls also closely resembled Canadians of the same age and sex, when compared with Census data in terms of parents' education, marital status, and household income.23 Scores of our control group are also similar to those obtained by Landgraf et al24 for their United States population aged 5 to 18 years, and are especially close for the white sample within that US cohort. Although our assessment of HRQL is based on parent-report only, and parents of children who have had cancer may be more attuned to potential issues with their children's physical and emotional health thus potentially biasing the results, this is not likely to be problematic in our study. Strong agreement exists between parent and adolescent self-report scores on the HRQL using the CHQ for groups of children on and off treatment for cancer.49 Parent-report has been found to be an adequate substitute for child-report at the group level, as used in our study, even though large differences can exist in individual child-parent agreement on children's HRQL.50 Finally, the physical domain, which is the aspect of HRQL where parent-report is most consistent with self-report,49 is the domain in which we found the most clinically important differences between survivors and controls. Although we found smaller survivor-control differences in the psychosocial domain, our use of parent-report means we cannot eliminate the possibility that there could still be effects in this domain that we were unable to detect. However, when we compared outcomes of adult survivors and controls using self-report as part of the Late Effects Study, we found the same pattern of results with differences primarily concentrated in the physical domain (Maunsell et al,51 in this issue of the Journal of Clinical Oncology). Our results contribute to knowledge about children and adolescents surviving cancer in several important ways. First, we moved beyond previous reports of the more traditional medical outcomes and individual psychosocial outcomes to assess HRQL using a single validated instrument that measures emotional and social dimensions in addition to physical dimensions. This is the first such report based on a large random sample of a diverse childhood-cancer population. We also identified the specific domains of HRQL that are particularly affected and the diagnostic and treatment subgroups most at risk for clinically meaningful deficits in HRQL. This information has not been available previously.34 Our use of a matched, general population control group overcomes the potential bias inherent in sibling controls associated with the effects that childhood cancer can have on siblings. This greater understanding should help guide the modification of treatment and inform the process of structuring comprehensive long-term follow-up of survivors, especially among survivors who have not yet reached adulthood.12,13,52,53
Participating centers and agencies. British Columbia Cancer Agency, British Columbia Children's Hospital, Alberta Cancer Board, Alberta Children's Hospital, Cross Cancer Institute, Saskatchewan Cancer Agency, Allan Blair Cancer Centre, Saskatoon Cancer Centre, Manitoba Cancer Treatment and Research Foundation, Chedoke-McMaster Hospital, Hospital for Sick Children, Hôpital Ste-Justine, Montréal Children's Hospital, Isaac Walton Killam Children's Hospital, and Janeway Child Health Centre.
The authors indicated no potential conflicts of interest.
We thank the past members of the Canadian Childhood Cancer Surveillance and Control Program Late Effects Working Group and Management Committee, the participating centers and agencies (see Appendix), the participants who generously gave their time to participate, and Jamie Seabrook for assistance in the final preparation of this manuscript.
Supported by Health Canada. E.M. was a National Health Research and Development Program (NHRDP) National Health Research Scholar and an Investigator of the Canadian Institutes of Health Research (CIHR) when this study was planned, conducted, and analyzed. Authors' disclosures of potential con- flicts of interest and author contributions are found at the end of this article.
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Copyright © 2006 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
= .05) used in this analysis was adjusted with the Bonferroni correction (0.05/10 scale scores compared, or 0.005). All independent variables (listed in 
