Healthy lifestyle including sufficient physical activity may mitigate or prevent adverse long-term effects of childhood cancer. We described daily physical activities and sports in childhood cancer survivors and controls, and assessed determinants of both activity patterns.
The Swiss Childhood Cancer Survivor Study is a questionnaire survey including all children diagnosed with cancer 1976–2003 at age 0–15 years, registered in the Swiss Childhood Cancer Registry, who survived ≥5years and reached adulthood (≥20years). Controls came from the population-based Swiss Health Survey. We compared the two populations and determined risk factors for both outcomes in separate multivariable logistic regression models. The sample included 1058 survivors and 5593 controls (response rates 78% and 66%). Sufficient daily physical activities were reported by 52% (n = 521) of survivors and 37% (n = 2069) of controls (p<0.001). In contrast, 62% (n = 640) of survivors and 65% (n = 3635) of controls reported engaging in sports (p = 0.067). Risk factors for insufficient daily activities in both populations were: older age (OR for ≥35years: 1.5, 95CI 1.2–2.0), female gender (OR 1.6, 95CI 1.3–1.9), French/Italian Speaking (OR 1.4, 95CI 1.1–1.7), and higher education (OR for university education: 2.0, 95CI 1.5–2.6). Risk factors for no sports were: being a survivor (OR 1.3, 95CI 1.1–1.6), older age (OR for ≥35years: 1.4, 95CI 1.1–1.8), migration background (OR 1.5, 95CI 1.3–1.8), French/Italian speaking (OR 1.4, 95CI 1.2–1.7), lower education (OR for compulsory schooling only: 1.6, 95CI 1.2–2.2), being married (OR 1.7, 95CI 1.5–2.0), having children (OR 1.3, 95CI 1.4–1.9), obesity (OR 2.4, 95CI 1.7–3.3), and smoking (OR 1.7, 95CI 1.5–2.1). Type of diagnosis was only associated with sports.
Citation: Rueegg CS, von der Weid NX, Rebholz CE, Michel G, Zwahlen M, Grotzer M, et al. (2012) Daily Physical Activities and Sports in Adult Survivors of Childhood Cancer and Healthy Controls: A Population-Based Questionnaire Survey. PLoS ONE 7(4): e34930. https://doi.org/10.1371/journal.pone.0034930
Editor: Alejandro Lucia, Universidad Europea de Madrid, Spain
Received: November 28, 2011; Accepted: March 7, 2012; Published: April 10, 2012
Copyright: © 2012 Rueegg et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was supported by the Swiss Cancer League (Grant No KLS-01605-10-2004 and KLS-2215-02-2008; www.krebsliga.ch), Bernese Cancer League (www.bernischekrebsliga.ch), Cancer League Zurich (www.krebsliga-zh.ch), Swiss Bridge (www.swissbridge.ch), and Stiftung zur Krebsbekämpfung (www.krebsbekaempfung.ch). GM and CEK were funded by the Swiss National Science Foundation (GM: Fellowship grant PA001-117433/1; CEK: PROSPER grant 3233-069348; www.snf.ch). CR was funded by the Bernese Cancer League (Berner Krebsstipendium 2010; www.bernischekrebsliga.ch). The work of the Swiss Childhood Cancer Registry is supported by the Swiss Paediatric Oncology Group (www.spog.ch), Kinderkrebshilfe Schweiz (www.kinderkrebshilfe.ch), Stiftung für krebskranke Kinder Regio Basiliensis (www.krebskrankekinder.ch), Novartis Oncology Switzerland (www.novartisoncology.ch), Interpharma (www.interpharma.ch), Axa Wintherthur (www.axa-winterthur.ch), Glaxo Smithkline (www.glaxosmithkline.ch), Amgen (www.amgen.ch), Bristol Myers Squibb (www.bms.ch) and numerous other sponsors. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Survival rates of childhood cancer reached 80% , , resulting in a growing population of adult childhood cancer survivors. This has shifted to some extent the focus of childhood cancer treatment and its follow-up from saving the patient's life to preserving long-term health. Due to genetic predisposition or therapy, childhood cancer survivors are at increased risk for developing late effects such as pain, fatigue, obesity, diabetes, cardiovascular diseases, osteoporosis, cognitive problems, neuro-musculoskeletal complications, low functional capacity or late mortality , , , , , . An active lifestyle has been shown to mitigate or prevent these problems in childhood cancer survivors , , , , , , , , survivors of adult cancer , ,  and animal studies .
Two main types of physical activities have been described: 1) moderate or vigorous activities of daily living such as cleaning, gardening, walking, cycling or climbing stairs, labeled here as “daily activities”; and 2) targeted sports practiced on a regular basis such as soccer, jogging or gymnastics, labeled in this paper as “sports”. For health benefits, international guidelines recommend at least 30 minutes of moderate activities on at least 5 days per week or 20 minutes of vigorous activities on at least 3 days per week . Increasing time of physical activity was shown to provide even greater health benefits , .
Despite its importance for maintenance of general health, relatively little is known about activity patterns of adult survivors of childhood cancer , . Studies from the USA showed varying proportions of active survivors (between 36% and 80%) , , , , , . Two of them compared results to healthy controls and distinguished between different types of physical activities , . Four studies assessed determinants of physical activity; their results were inconsistent , , , , . For Europe, we only found one report on physical activity in European childhood cancer survivors. This was a single-center study conducted in Finland based on a small sample of 21 survivors and controls .
We analyzed data from the nationwide Swiss Childhood Cancer Survivor Study and population-based controls from the Swiss Health Survey to compare daily activities and sports between the two populations, and to determine risk factors for insufficient daily activities and lack of sports.
Materials and Methods
Ethics approval was provided through the general cancer registry permission of the Swiss Childhood Cancer Registry (The Swiss Federal Commission of Experts for Professional Secrecy in Medical Research) and a non obstat statement was obtained from the ethics committee of the canton of Bern, stating that no additional informed consent was necessary for the Swiss Childhood Cancer Survivor Study. All information regarding individuals from the Swiss Childhood Cancer Survivor Study as well as the Swiss Health Survey was made anonymous to investigators prior to analysis.
The Swiss Childhood Cancer Survivor Study (SCCSS)
The SCCSS is a population-based long-term follow-up study of all childhood cancer patients registered in the Swiss Childhood Cancer Registry (SCCR), diagnosed between 1976 and 2003 at an age of 0–15 years, who survived at least 5 years . The SCCR includes all children and adolescents in Switzerland diagnosed with leukemia, lymphoma, central nervous system (CNS) tumors, malignant solid tumors or Langerhans cell histiocytosis before age16 years , .
In 2007–2009, eligible study participants (N = 1686) were traced with an extensive address search procedure. They received an information letter from their former pediatric oncology clinic, followed by a questionnaire with a pre-paid return envelope. Non-responders received a second questionnaire four weeks later and were then reminded by phone. Letters and questionnaires were provided in three national languages: German, French and Italian (http://www.childhoodcancerregistry.ch/sccss). The SCCSS used an extensive questionnaire derived from the US and British childhood cancer survivor studies , . Questions on health behaviors and socio-demographic measures were added from the Swiss Health Survey 2007  and the Swiss Census 2000 , to allow comparisons with the Swiss general population. The main domains of the questionnaire were: quality of life, somatic health, fertility, current medication and health service utilization, psychological distress, health behaviors, and socio-economic information.
The Swiss Health Survey (SHS)
The SHS is a periodical (every 5 years), representative telephone survey to describe the state of health and related questions of the Swiss resident population. We used data from the 2007 survey. Detailed information on the study procedure and questionnaire are provided on the homepage of the Swiss Statistics (http://www.bfs.admin.ch/bfs/portal/de/index/infothek/erhebungen__quellen/blank/blank/ess/03.html). Briefly, a random sample was obtained by stratified selection on two stages: in the first stage, households were randomly selected from each canton with oversampling in 14 cantons. In the second stage one person was randomly selected in each household. The sampling list consisted of 30'179 addresses of households. Thereof 1847 addresses were not valid. Of the remaining 28'332 households, 6185 households were unavailable and 3414 persons refused to participate, resulting in a sample of 18'760 interviewed persons (response rate 66%) . The interview of participants was done by a computer assisted phone interview (CATI). The questionnaire included close to 400 questions grouped in 69 domains, which comprised questions on socio-demographic and socio-economic status, on health status, health related behaviours and health related attitudes as well as on the utilisation of health services. For this study, we only included SHS respondents aged 20–40 years according to the age range of survivors (n = 5593).
Assessment of physical activity
- “Daily activities”: first, all participants were asked on how many days per week they engage in any type of activities that make them sweat (vigorous activities). Survivors were also asked how many minutes per day they engage in such activities. Then, participants were asked how many days per week and minutes per day they engage in activities that cause some increase in breathing (moderate activities). Examples were given for both types of activities in the questionnaires. People were then classified as “active” (vs. “inactive”) if they engaged in moderate activities for ≥30 minutes on ≥5 days a week or in vigorous activities on ≥3 days a week, according to the international physical activity recommendations of the Centers of Disease Control and Prevention (CDC) .
- “Sporting activities”: participants were asked whether they engage in any gymnastics, fitness training or sports; how intensely they practice these sports; and how many hours per week. People were then classified as doing “sports” (vs. “no sports”) if they engaged in a targeted gym or sport at least somewhat intense and at least one hour per week. Survivors were also asked to list the types of sport they were doing.
Information assessed by questionnaire
Explanatory variables assessed by questionnaire for both populations were: age at survey, gender, language region of Switzerland (German vs. French/Italian), civil status (married vs. single/divorced/other), having children, smoking status, migration background, education, and body mass index (BMI). Education was classified into four categories according to the Swiss Census: compulsory schooling only (≤9 years), vocational training (10–13 years), upper secondary education (higher vocational training or college), and university degree , . Participants were classified as having a migration background if they were not Swiss citizens since birth, were not born in Switzerland, or at least one of the parents was not Swiss citizen. BMI was classified as underweight (BMI<18 kg/m2), normal weight (≥18–24.9 kg/m2), overweight (≥25–29.9 kg/m2), and obese (≥30 kg/m2) . For survivors, self-reported late effects from cancer were assessed and coded into somatic or psychological late effects.
Information extracted from the Swiss Childhood Cancer Registry (SCCR)
Prospectively collected medical information on diagnosis and treatment of survivors was extracted from the SCCR: age at diagnosis, cancer diagnosis, treatments, and time since diagnosis. Treatment was classified as surgery only, chemotherapy with or without surgery, radiotherapy with or without chemotherapy or surgery, and bone marrow transplantation. Diagnosis was classified according to the International Classification of Childhood Cancer - 3rd Edition .
This analysis included all participants of the Swiss Childhood Cancer Survivor Study and the Swiss Health Survey aged 20 to 40 years at the time of survey. The Swiss Health Survey, our control population, included more migrants, French and Italian speaking, and older persons. On the combined data set we used multivariable logistic regression with being a control as outcome to compute appropriate weights to assure that the weighted marginal distribution of the control population for age, gender, language region, and migration background was identical to that in survivors (Table 1). The weight for the cancer survivors was set to one. We applied these weights in all analyses.
First, we used a combined dataset of survivors and controls to compare frequencies of outcomes and predictors using two-sample tests for proportions on Wald statistics. Means were compared using two-group comparison t-tests. We then fitted univariable and multivariable logistic regression models to determine associations of survivorship and other risk factors with the outcomes daily activities and sports. Variables that were significantly associated (p<0.05) with either of the two outcomes in the univariable model were included into the multivariable model. Wald tests were used to calculate global p-values. We used interaction tests to determine whether risk factors differed between the two populations, with a p<0.01 considered as statistically significant.
Second, we investigated associations between clinical factors (type of diagnosis and treatments) with the two types of physical activity, using the dataset of survivors only. P-values<0.05 were considered as statistically significant.
Analyses were performed with Stata, version 11.0 (Stata Corporation, Austin, Texas).
Characteristics of the study population
Addresses could be traced for 1487 of 1686 eligible survivors (Figure 1). Of those traced, 1156 (78%) returned a questionnaire, 1058 (71%) the full-length questionnaire and 98 (7%) an abbreviated version without questions on physical activity. Participants (n = 1058), in comparison to non-participants (n = 628), were more often female (47% vs. 38%) (p = <0.001), less often French (20% vs. 29%) or Italian (3% vs. 4%) speaking (p<0.001), had had more often leukemia (37% vs. 29%) (p = 0.008), and chemotherapy (47% vs. 44%) or bone marrow transplantation (8% vs. 3%) (p<0.001) (Table S1). They did not differ by current age, age at diagnosis, and time since diagnosis.
Flow diagram of our study population starting from those eligible in the Swiss Childhood Cancer Registry to those included in the analysis.
Compared to controls (Table 1), more survivors had compulsory schooling only (9% vs. 6%) or upper secondary education (35% vs. 15%), and fewer had vocational training (49% vs. 65%) or a university degree (7% vs. 14%; p<0.001). Fewer survivors were married (17% vs. 26%), had children (13% vs. 54%), or were current smoker (24% vs. 39%; all p<0.001). Mean BMI did not differ between the groups, but more survivors were underweight, overweight or obese (p = 0.001).
Most survivors had suffered from leukemia (37%), lymphoma (21%) or a CNS tumor (11%), 36% had been treated by radiotherapy and 8% with bone marrow transplant (Table 1). Mean age at diagnosis was 8.3 years (SD 4.8 years) and mean time elapsed since diagnosis 19.5 years (SD 6.6 years). About one third reported to suffer from late effects of their cancer disease.
Daily activities and sports in survivors and controls
Sufficient daily activities were reported by 52% (n = 521) of survivors and 37% (n = 2069) of controls (p<0.001, Figure 2). Sports participation was reported by 62% (n = 640) of survivors and 65% (n = 3635) of controls (p = 0.067). Survivors and controls had a similar proportion (21%) of completely inactive individuals, who neither engaged in sufficient daily activities nor in sports (data not shown). Survivors engaged in all typical types of sports, namely fitness training (reported by n = 385), outdoor activities (n = 170), ball games (n = 108), water sports (n = 97), rebounding ball games (n = 77), winter sports (n = 65), and others (n = 67; data not shown).
Proportions of persons 1) meeting (active) or not meeting (inactive) healthy recommendations for daily activities, and 2) participating (sports) or not participating (no sports) in sporting activities, for childhood cancer survivors compared to the weighted proportions of healthy controls (p<0.001 for daily activities, and p = 0.067 for sports, comparing survivors and controls). * Weighted proportions and numbers for controls: adjusted for age, gender, language region, and migration background.
Determinants of daily activities
Determinants of insufficient daily activities in a univariable logistic regression were: female sex (OR 1.6, 95CI 1.4–1.8), older age (OR for ≥35 years: 1.5, 95CI 1.2–1.9), higher education (OR for university degree: 2.3, 95CI 1.8–3.0), being married (OR 1.3, 95CI 1.1–1.6), having children (OR 1.3, 95CI 1.1–1.5), living in the French or Italian speaking part of Switzerland (OR 1.4, 95CI 1.2–1.6) and being underweight (OR 1.9, 95CI 1.2–3.1) (Table S2). Not associated were: migration background and smoking. Adjusting for all these variables, fewer survivors than controls reported insufficient daily activities (OR 0.5, 95CI 0.4–0.6) (Table 2). With the exception of civil status and having children all other variables remained associated in the adjusted model. Associations between risk factors and outcomes were similar for survivors and healthy peers. All p values for interaction were >0.01 apart from language region (p<0.001) and BMI (p = 0.006). Only French and Italian speaking survivors but not controls were at risk for insufficient daily activities. BMI was only associated in controls but not in survivors.
Determinants of sporting activities
Determinants of sporting activities differed from determinants of daily activities (Figure 3). In the univariable model factors associated with lack of sports were: older age (OR for ≥35 years: 1.4, 95CI 1.1–1.8), female sex (OR 1.2, 95CI 1.0–1.4), migration background (OR 1.5, 95CI 1.3–1.8), French or Italian speaking (OR 1.4, 95CI 1.2–1.7), compulsory schooling only (OR 1.6, 95CI 1.2–2.2), being married (OR 1.7, 95CI 1.5–2.0), having children (OR 1.3, 95CI 1.1–1.5), being obese (OR 2.4, 95CI 1.7–3.3) and current smoking (OR 1.6, 95CI 1.4–1.9; Table S2). Participants with higher education participated more often in sports. Results from the multivariable model were similar to the univariable regression, only current age was no longer associated (Table 2). In contrast to daily activities, however, more survivors reported a lack of sporting activities (OR 1.3, 95CI 1.1–1.6). There was no evidence that the effect of risk factors differed between survivors and their peers (all p values for interaction >0.01).
Effect sizes for two different outcomes assessing physical activity derived from two multivariable regression models with a combined dataset including childhood cancer survivors and healthy controls. Abbreviations: OR, Odds Ratio. * versus age <25 years. † versus vocational training. ‡ versus normal weight.
Association between clinical factors and physical activities in survivors
Adjusting for all socio-demographic and cultural factors listed in Table 2, none of the clinical factors (type of diagnosis, age at diagnosis, treatments or self-reported late effects) were significantly associated with daily activities (results from univariable models in Table S3). However, there was a trend for lower activity levels in survivors of neuroblastomas, soft tissue sarcomas, and germ cell tumors (Table 3). The same was true for clinical predictors of sporting activities (results from univariable models in Table S3): while there was no statistically significant association with clinical factors, there was a trend (p = 0.087) for reporting less sports in survivors of bone tumors (OR 2.0, 95CI 1.1–3.9), germ cell tumors (OR 2.2, 95CI 0.9–5.3), CNS tumors (OR 1.6, 95CI 0.9–3.0), neuroblastomas (OR 1.8, 95CI 0.8–4.0), and retinoblastomas (OR 1.8, 95CI 0.6–5.3; Table 3).
To our knowledge, this is the first population based study that compared different types of physical activities between childhood cancer survivors and healthy controls in Europe. Results differed between the two types of activities: while survivors reported more daily activities, they performed fewer sports than controls. Risk factors for inactivity did also differ between daily activities and sports. Demographic and cultural factors such as gender, age, education, BMI, smoking status and family status were the most important determinants of physical activity in both populations.
Strengths and limitations
A major strength of our study is the population-based, representative and large sample of Swiss childhood cancer survivors. Thanks to the high response rate of 78%, selection bias plays a minor role. Demographic and medical information had been collected prospectively in the Swiss Childhood Cancer Registry. By weighting the analysis, we could compare proportions between the two populations which were standardized with respect to age, sex, nationality, and language region, allowing a valid comparison between survivors and controls. Finally, same questions had been used to assess outcomes and exposures in both studies.
There are some limitations to be acknowledged regarding the assessment of physical activities. First, a clear limitation, which this study shares with others , , , ,  is, that physical activity was self-reported. Physical activity can only incompletely be assessed by questionnaire, and social desirability bias and subjective interpretation has to be considered. The current gold standard for assessment of physical activity is doubly labeled water , but the method is costly and rarely used. A second possibility is the use of accelerometers . The questions on daily activities we used in our survey are internationally standardized and had been validated against accelerometer assessment in childhood cancer survivors with good correlations , . The questions on sports have been used in the Swiss Health Survey since 1997 . Second, a problem in the assessment of daily activities is, that the duration (minutes) of vigorous activities was not assessed in the control population, as it was assumed in the Swiss Health Survey that engagement in vigorous activities virtually always lasts more than 20 minutes. We used the same classification strategy for survivors and controls, neglecting the minutes of vigorous activities. This might have led to a slight overestimation of the daily activities but allows a fair comparison of the two populations. Third, we cannot fully separate daily activities and sports with the questions used. There might be some degree of overlapping. Despite this, there is evidence for clearly different risk profiles for daily activities and sports (Figure 3). Had we been able to make a clearer distinction between the two outcomes, the differences in risk factors would likely have been more extreme. Last, we cannot exclude that the different survey designs (written questionnaire in survivors, telephone interview in controls) might have influenced the results, with responders to the telephone survey being more prone to social desirability bias .
Finally, although it was a nationwide survey, the relative rarity of childhood cancer resulted in limited numbers of participants and thus limited power to show small differences between diagnostic groups.
Comparison with other studies
Two studies from the US Childhood Cancer Survivor Study previously studied daily activities in a population-based sample of adult childhood cancer survivors, using similar questions and classifications , . In contrast to our study, Ness et al. found that less survivors than controls engaged in sufficient daily activities. Among 9301 survivors of the Childhood Cancer Survivor Study compared to 2886 siblings, 45% survivors and 51% siblings reported sufficient daily activities . This was slightly lower than among 2'648 adult survivors of ALL who participated in the Childhood Cancer Survivor Study compared to 110'623 controls from the Behavioral Risk Factor Surveillance System of the USA. In this group, 48% survivors and 52% controls reported sufficient daily activities .
These two studies also compared sporting activities, although assessed slightly different. Overall, the proportion engaging in sports was lower in the US studies than in our findings from Switzerland, both in survivors and controls. However, consistent with our findings fewer survivors than controls engaged in sports , . In the study of Florin et al. 77% survivors reported no sports compared to 80% controls; Ness et al. reported 77% vs. 86%, respectively. Ness et al. found similar associations between sports and socio-demographic factors as we did in Switzerland (age, education, BMI, smoking), but also associations with certain diagnoses (medullablastoma and osteosarcoma) and treatments (cranial radiation or amputation).
Differences between our findings and those from the US might be explained by socio-demographic, clinical and cultural differences between Swiss and US survivors and controls, as well as differences in the information on diagnosis and treatment.
Interpretation of the results
We found that risk factors for physical activity and comparisons between survivors and controls depend on the definition of the outcome, e.g. the way physical activity is assessed. Survivors reported more daily activities but fewer sports than their peers. In both survivors and controls, socio-demographic and cultural factors were important determinants of activity patterns, but they differed by type of activity (Figure 3, Table 2).
Previous studies found that higher education positively influences physical activity . We confirmed this in our study for sporting activities. The inverse association we found between educational level and daily activities might be explained by more sedentary work and more working hours per day in higher educated persons.
In the analysis including childhood cancer survivors only, socio-demographic and cultural factors remained the main determinants of activity patterns, and clinical factors played a comparatively minor role. Only for the outcome “sports”, we found a disadvantage for survivors of certain types of cancers: bone tumors, germ cell tumors, retinoblastomas, neuroblastomas and CNS tumors. This might be due to cancer- or treatment related short- or long-term effects that impede participation in many sports, such as vision impairments after retinoblastoma, leg amputation after bone tumor or problems with balance or coordination after a CNS tumor.
In contrast, more survivors than controls reported sufficient daily activities. Perhaps survivors who cannot participate in targeted sports, due to performance limitations  or because of the “overprotected child syndrome” , they try to compensate this by including more activities into daily living. Alternatively it could be explained by the way daily activities are measured in the standardized instrument that we used, i.e. as “activities that make you breathe or sweat”. Survivors with physical handicaps, might tend to “breathe hard or sweat” more easily than peers during normal activities of daily living. A last potential explanation is selection bias: survivors in poor health might be both less likely to complete the questionnaire and to perform sports. These considerations might explain why the picture we gain from this survey contrasts with impressions from follow-up clinics, where survivors with the poorest outcomes are most likely to be seen.
Implication for practice
Several intervention studies during or right after treatment of childhood cancer patients with promising results are mentioned in the literature , , . However, only little is known on interventions that target enhancement of physical activity levels in adult survivors of childhood cancer many years after completion of treatment . Therefore, our findings can inform daily practice and should feed into physical activity counseling during follow-up visits of current patients and long term survivors. Clinicians should keep in mind that several types of physical activity exist and risk profiles for inactivity differ depending on the type of activity. Depending on clinical factors (limitations for certain types of activities), individual preferences or risk profiles, different types of activities should be proposed to improve life-long engagement in physical activity.
For instance, survivors with certain performance-limiting late effects such as amputations or overweight that keep them from participating in certain sporting activities, could instead be motivated to include moderate physical activities into their daily living. From a health perspective, this type of moderate activity is sufficient to reduce the risk for chronic diseases , . Thus, clinicians could give ideas on how to integrate activity into daily living: for example, climbing stairs instead of taking the elevator, riding a bicycle instead of taking a car, getting out of the bus a station earlier and walk the last meters, or balance on one leg while brushing teeth.
Importantly, the same socio-demographic and cultural factors determined activity patterns in survivors and their peers. This suggests that strategies to motivate childhood cancer survivors to be more active and structures to facilitate healthy activity behavior could be essentially similar as for the general population. Former patients can and should be integrated into physical activity interventions that aim for the general population, such as health-promoting school or work place interventions . This does not exclude that high risk patients, such as those with multiple morbidities or those at high risk for cardiovascular, musculoskeletal, and neurocognitive late effects should be identified early and offered multiple health behavior counseling on an individual basis.
Physical activity is a powerful tool to prevent chronic diseases and increases quality of life in healthy people , , . Due to the vulnerability of cancer survivors and their high risk for chronic disease after treatment, a healthy lifestyle including regular physical activity is particularly important for this population , , , , . Although we found that childhood cancer survivors were at least as active as their healthy peers, 48% did not reach recommended daily activity levels, 37% reported not doing any sports, and 21% reached neither recommendations for daily activities nor engaged in sports. These survivors are at a higher risk for developing late effects such as low bone mineral density, obesity, fatigue, cardiovascular diseases, low health related quality of life, or neurocognitive decline , , , , , . As health behaviors tend to cluster together, inactive survivors might also be more prone to engage in other health compromising behaviors such as smoking, drinking or unhealthy diet . This underlines the necessity to promote physical activity in childhood cancer survivors already early in follow-up. In addition, because risk factors for inactivity are essentially similar as in peers, survivors will benefit from all strategies that promote sports and daily physical activity in the general population.
Questions on physical activity from the Swiss Childhood Cancer Survivor Study questionnaire (translated into English). Same questions were asked to the controls in the Swiss Health Survey, excluding question 2 and 6.
Characteristics of participants included in the analysis and non-participantsa. Abbreviations: ICCC-3, International Classification of Childhood Cancer Third Edition; CNS, Central Nervous System; SD, Standard Deviation. a non-participants included: survivors without current address (n = 199), who did not response (n = 252), who refused to participate (n = 79), who answered an abridged questionnaire (n = 98). b p-value calculated from chi-square statistics. c other malignant epithelial neoplasms, malignant melanomas and other or unspecified malignant neoplasms. d chemotherapy may include surgery. e radiotherapy may include chemotherapy or surgery. f p-value calculated from two-group mean-comparison test (t-test).
Risk factors for inactivity and no sports from unadjusted regression modelsa (combined dataset including childhood cancer survivors and controls). Abbreviations: BMI, Body Mass Index; CI, Confidence Interval; OR, Odds Ratio. a calculated on weighted analysis (weights on: age, gender, language region, nationality). b standardized proportions given in column percentages. c global p-value calculated with a Wald test.
Risk factors for inactivity and no sports in childhood cancer survivors from unadjusted regression models. Abbreviations: BMI, Body Mass Index; BMT, Bone Marrow Transplantation; Chemo, Chemotherapy; CI, Confidence Interval; CNS, Central Nervous System; ICCC-3, International Classification of Childhood Cancer Third Edition; OR, Odds Ratio; Radio, Radiotherapy. a column percentages are given. b global p-value calculated with a Wald test. c chemotherapy may include surgery. d radiotherapy may include chemotherapy or surgery. e renal and hepatic tumors have been merged for this analysis. f other malignant epithelial neoplasm, malignant melanomas and other or unspecified malignant neoplasm.
We thank the Swiss Statistics for providing the data of the Swiss Health Survey 2007 for this analysis as well as all survivors and their families for participating in our survey. We thank the Swiss Pediatric Oncology Group (SPOG) Scientific Committee: Prof. Dr. med. R. Ammann, Bern; Dr. med. R. Angst, Aarau; PD Dr. med. M. Beck Popovic, Lausanne; Dr. med. P. Brazzola, Bellinzona; Dr. med. U. Caflisch, Lucerne; Dr. med. J. Greiner, St. Gallen; Prof. Dr. med. M. Grotzer, Zurich; Dr. med. H. Hengartner, St. Gallen; Prof. Dr. med. T. Kühne, Basel; Prof. Dr. med. K. Leibundgut, Bern; Prof. Dr. med. F. Niggli, Zürich; Dr. med. L. Nobile Buetti, Locarno; PD Dr. med. H. Ozsahin, Geneva; Prof. Dr. med. M. Paulussen, Basel; PD Dr. med. J. Rischewski, Lucerne; PD Dr. med. N. von der Weid, Lausanne.
Conceived and designed the experiments: CSR NXvdW CER GM MZ MG CEK. Performed the experiments: CSR CER GM CEK. Analyzed the data: CSR NXvdW CER GM MZ MG CEK. Contributed reagents/materials/analysis tools: CSR GM MZ CEK. Wrote the paper: CSR NXvdW CER GM MZ MG CEK.
- 1. Gatta G, Zigon G, Capocaccia R, Coebergh JW, Desandes E, et al. (2009) Survival of European children and young adults with cancer diagnosed 1995–2002. European Journal of Cancer 45: 992–1005.G. GattaG. ZigonR. CapocacciaJW CoeberghE. Desandes2009Survival of European children and young adults with cancer diagnosed 1995–2002.European Journal of Cancer459921005
- 2. Jemal A, Siegel R, Xu J, Ward E (2010) Cancer Statistics, 2010. CA Cancer J Clin 60: 277–300.A. JemalR. SiegelJ. XuE. Ward2010Cancer Statistics, 2010.CA Cancer J Clin60277300
- 3. Oeffinger KC, Mertens AC, Sklar CA, Kawashima T, Hudson MM, et al. (2006) Chronic Health Conditions in Adult Survivors of Childhood Cancer. New England Journal of Medicine 355: 1572–1582.KC OeffingerAC MertensCA SklarT. KawashimaMM Hudson2006Chronic Health Conditions in Adult Survivors of Childhood Cancer.New England Journal of Medicine35515721582
- 4. Alvarez JA, Scully RE, Miller TL, Armstrong FD, Constine LS, et al. (2007) Long-term effects of treatments for childhood cancers. Current Opinion in Pediatrics 19: 23–31.JA AlvarezRE ScullyTL MillerFD ArmstrongLS Constine2007Long-term effects of treatments for childhood cancers.Current Opinion in Pediatrics192331
- 5. Diller L, Chow EJ, Gurney JG, Hudson MM, Kadin-Lottick NS, et al. (2009) Chronic Disease in the Childhood Cancer Survivor Study Cohort: A Review of Published Findings. Journal of Clinical Oncology 27: 2339–2355.L. DillerEJ ChowJG GurneyMM HudsonNS Kadin-Lottick2009Chronic Disease in the Childhood Cancer Survivor Study Cohort: A Review of Published Findings.Journal of Clinical Oncology2723392355
- 6. Mertens AC, Liu Q, Neglia JP (2008) Cause-specific late mortality among 5-year survivors of childhood cancer: the Childhood Cancer Survivor Study. J Natl Cancer Inst 100: 1368–1379.AC MertensQ. LiuJP Neglia2008Cause-specific late mortality among 5-year survivors of childhood cancer: the Childhood Cancer Survivor Study.J Natl Cancer Inst10013681379
- 7. Reulen RC, Winter DL, Frobisher C, Lancashire ER, Stiller CA, et al. (2010) Long-term Cause-Specific Mortality Among Survivors of Childhood Cancer. JAMA: The Journal of the American Medical Association 304: 172–179.RC ReulenDL WinterC. FrobisherER LancashireCA Stiller2010Long-term Cause-Specific Mortality Among Survivors of Childhood Cancer.JAMA: The Journal of the American Medical Association304172179
- 8. San Juan AF, Chamorro-Viña C, Maté-Muñoz JL, Fernández del Valle M, Cardona C, et al. (2008) Functional capacity of children with leukemia. Int J Sports Med 29: 163–167.AF San JuanC. Chamorro-ViñaJL Maté-MuñozM. Fernández del ValleC. Cardona2008Functional capacity of children with leukemia.Int J Sports Med29163167
- 9. Blaauwbroek R, Bouma M, Tuinier W, Groenier K, de Greef M, et al. (2009) The effect of exercise counselling with feedback from a pedometer on fatigue in adult survivors of childhood cancer: a pilot study. Supportive Care in Cancer 17: 1041–1048.R. BlaauwbroekM. BoumaW. TuinierK. GroenierM. de Greef2009The effect of exercise counselling with feedback from a pedometer on fatigue in adult survivors of childhood cancer: a pilot study.Supportive Care in Cancer1710411048
- 10. Hartman A, Winkel MLt, Beek RDv, Keizer-Schrama SMPFdM, Kemper HCG, et al. (2009) A randomized trial investigating an exercise program to prevent reduction of bone mineral density and impairment of motor performance during treatment for childhood acute lymphoblastic leukemia. Pediatric Blood & Cancer 53: 64–71.A. HartmanMLt WinkelRDv BeekSMPFdM Keizer-SchramaHCG Kemper2009A randomized trial investigating an exercise program to prevent reduction of bone mineral density and impairment of motor performance during treatment for childhood acute lymphoblastic leukemia.Pediatric Blood & Cancer536471
- 11. Mayer EIE, Reuter M, Dopfer RE, Ranke MB (2000) Energy Expenditure, Energy Intake and Prevalence of Obesity after Therapy for Acute Lymphoblastic Leukemia during Childhood. Hormone Research in Paediatrics 53: 193–199.EIE MayerM. ReuterRE DopferMB Ranke2000Energy Expenditure, Energy Intake and Prevalence of Obesity after Therapy for Acute Lymphoblastic Leukemia during Childhood.Hormone Research in Paediatrics53193199
- 12. Meacham LR, Chow EJ, Ness KK, Kamdar KY, Chen Y, et al. (2010) Cardiovascular Risk Factors in Adult Survivors of Pediatric Cancer—A Report from the Childhood Cancer Survivor Study. Cancer Epidemiology Biomarkers & Prevention 19: 170–181.LR MeachamEJ ChowKK NessKY KamdarY. Chen2010Cardiovascular Risk Factors in Adult Survivors of Pediatric Cancer—A Report from the Childhood Cancer Survivor Study.Cancer Epidemiology Biomarkers & Prevention19170181
- 13. San Juan AF, Fleck SJ, Chamorro-Viña C, Maté-Muñoz JL, Moral S, et al. (2007) Effects of an intrahospital exercise program intervention for children with leukemia. Med Sci Sports Exerc 39: 13–21.AF San JuanSJ FleckC. Chamorro-ViñaJL Maté-MuñozS. Moral2007Effects of an intrahospital exercise program intervention for children with leukemia.Med Sci Sports Exerc391321
- 14. San Juan AF, Wolin K, Lucía A (2011) Physical Activity and Pediatric Cancer Survivorship. Recent Results Cancer Res 186: 319–347.AF San JuanK. WolinA. Lucía2011Physical Activity and Pediatric Cancer Survivorship.Recent Results Cancer Res186319347
- 15. Tillmann V, Darlington ASE, Eiser C, Bishop NJ, Davies HA (2002) Male Sex and Low Physical Activity Are Associated With Reduced Spine Bone Mineral Density in Survivors of Childhood Acute Lymphoblastic Leukemia. Journal of Bone and Mineral Research 17: 1073–1080.V. TillmannASE DarlingtonC. EiserNJ BishopHA Davies2002Male Sex and Low Physical Activity Are Associated With Reduced Spine Bone Mineral Density in Survivors of Childhood Acute Lymphoblastic Leukemia.Journal of Bone and Mineral Research1710731080
- 16. van Brussel M, van der Net J, Hulzebos E, Helders PJM, Takken T (2011) The Utrecht Approach to Exercise in Chronic Childhood Conditions: The Decade in Review. Pediatric Physical Therapy 23: 2–14.M. van BrusselJ. van der NetE. HulzebosPJM HeldersT. Takken2011The Utrecht Approach to Exercise in Chronic Childhood Conditions: The Decade in Review.Pediatric Physical Therapy23214
- 17. Demark-Wahnefried W, Aziz NM, Rowland JH, Pinto BM (2005) Riding the Crest of the Teachable Moment: Promoting Long-Term Health After the Diagnosis of Cancer. J Clin Oncol 23: 5814–5830.W. Demark-WahnefriedNM AzizJH RowlandBM Pinto2005Riding the Crest of the Teachable Moment: Promoting Long-Term Health After the Diagnosis of Cancer.J Clin Oncol2358145830
- 18. Speck R, Courneya K, Mâsse L, Duval S, Schmitz K (2010) An update of controlled physical activity trials in cancer survivors: a systematic review and meta-analysis. Journal of Cancer Survivorship 4: 87–100.R. SpeckK. CourneyaL. MâsseS. DuvalK. Schmitz2010An update of controlled physical activity trials in cancer survivors: a systematic review and meta-analysis.Journal of Cancer Survivorship487100
- 19. Schmitz KH, Courneya KS, Matthews C, Demark-Wahnefried W, Galvao DA, et al. (2010) American College of Sports Medicine Roundtable on Exercise Guidelines for Cancer Survivors. Medicine & Science in Sports & Exercise 42: 1409–1426.KH SchmitzKS CourneyaC. MatthewsW. Demark-WahnefriedDA Galvao2010American College of Sports Medicine Roundtable on Exercise Guidelines for Cancer Survivors.Medicine & Science in Sports & Exercise4214091426
- 20. Naylor AS, Bull C, Nilsson MKL, Zhu C, Björk-Eriksson T, et al. (2008) Voluntary running rescues adult hippocampal neurogenesis after irradiation of the young mouse brain. Proceedings of the National Academy of Sciences 105: 14632–14637.AS NaylorC. BullMKL NilssonC. ZhuT. Björk-Eriksson2008Voluntary running rescues adult hippocampal neurogenesis after irradiation of the young mouse brain.Proceedings of the National Academy of Sciences1051463214637
- 21. Haskell WL, Lee IM, Pate RR, Powel KE, Bair SN, et al. (2007) Physical Activity and Public Health: Updated Recommendation for Adults from the American College of Sports Medicine and the American Heart Association. Medicine & Science in Sports & Exercise 39: 1423–1434.WL HaskellIM LeeRR PateKE PowelSN Bair2007Physical Activity and Public Health: Updated Recommendation for Adults from the American College of Sports Medicine and the American Heart Association.Medicine & Science in Sports & Exercise3914231434
- 22. Samitz G, Egger M, Zwahlen M (2011) Domains of physical activity and all-cause mortality: systematic review and dose–response meta-analysis of cohort studies. International Journal of Epidemiology 40: 1382–1400.G. SamitzM. EggerM. Zwahlen2011Domains of physical activity and all-cause mortality: systematic review and dose–response meta-analysis of cohort studies.International Journal of Epidemiology4013821400
- 23. Stolley M, Restrepo J, Sharp L (2010) Diet and Physical Activity in Childhood Cancer Survivors: A Review of the Literature. Annals of Behavioral Medicine 39: 232–249.M. StolleyJ. RestrepoL. Sharp2010Diet and Physical Activity in Childhood Cancer Survivors: A Review of the Literature.Annals of Behavioral Medicine39232249
- 24. Florin TA, Fryer GE, Miyoshi T, Weitzman M, Mertens AC, et al. (2007) Physical Inactivity in Adult Survivors of Childhood Acute Lymphoblastic Leukemia: A Report from the Childhood Cancer Survivor Study. Cancer Epidemiology Biomarkers & Prevention 16: 1356–1363.TA FlorinGE FryerT. MiyoshiM. WeitzmanAC Mertens2007Physical Inactivity in Adult Survivors of Childhood Acute Lymphoblastic Leukemia: A Report from the Childhood Cancer Survivor Study.Cancer Epidemiology Biomarkers & Prevention1613561363
- 25. Ness KK, Leisenring WM, Huang S, Hudson MM, Gurney JG, et al. (2009) Predictors of inactive lifestyle among adult survivors of childhood cancer. Cancer 115: 1984–1994.KK NessWM LeisenringS. HuangMM HudsonJG Gurney2009Predictors of inactive lifestyle among adult survivors of childhood cancer.Cancer11519841994
- 26. Finnegan L, Wilkie D, Wilbur J, Campbell R, Zong S, et al. (2007) Correlates of Physical Activity in Young Adult Survivors of Childhood Cancers. Oncology Nursing Forum 34: E60–E69.L. FinneganD. WilkieJ. WilburR. CampbellS. Zong2007Correlates of Physical Activity in Young Adult Survivors of Childhood Cancers.Oncology Nursing Forum34E60E69
- 27. Reeves M, Eakin EG, Lawler S, Demark-Wahnefried W (2007) Health behaviours in survivors of childhood cancer. Australian Family Physician 36: 95–96.M. ReevesEG EakinS. LawlerW. Demark-Wahnefried2007Health behaviours in survivors of childhood cancer.Australian Family Physician369596
- 28. Demark-Wahnefried W, Werner C, Clipp EC, Guill AB, Bonner M, et al. (2005) Survivors of childhood cancer and their guardians. Cancer 103: 2171–2180.W. Demark-WahnefriedC. WernerEC ClippAB GuillM. Bonner2005Survivors of childhood cancer and their guardians.Cancer10321712180
- 29. Cox CL, Montgomery M, Oeffinger KC, Leisenring W, Zeltzer L, et al. (2009) Promoting physical activity in childhood cancer survivors. Cancer 115: 642–654.CL CoxM. MontgomeryKC OeffingerW. LeisenringL. Zeltzer2009Promoting physical activity in childhood cancer survivors.Cancer115642654
- 30. Järvelä LS, Niinikoski H, Lähteenmäki PM, Heinonen OJ, Kapanen J, et al. (2010) Physical activity and fitness in adolescent and young adult long-term survivors of childhood acute lymphoblastic leukaemia. J Cancer Surviv 4: 339–345.LS JärveläH. NiinikoskiPM LähteenmäkiOJ HeinonenJ. Kapanen2010Physical activity and fitness in adolescent and young adult long-term survivors of childhood acute lymphoblastic leukaemia.J Cancer Surviv4339345
- 31. Kuehni CE, Rueegg CS, Michel G, Rebholz CE, Strippoli MPF, et al. (2011) Cohort profile: The Swiss Childhood Cancer Survivor Study. International Journal of Epidemiology. CE KuehniCS RueeggG. MichelCE RebholzMPF Strippoli2011Cohort profile: The Swiss Childhood Cancer Survivor Study.International Journal of Epidemiology ahead of print:.
- 32. Michel G, von der Weid NX, Zwahlen M, Adam M, Rebholz CE, et al. (2007) The Swiss Childhood Cancer Registry: rationale, organisation and results for the years 2001–2005. Swiss Medical Weekly 137: 502–509.G. MichelNX von der WeidM. ZwahlenM. AdamCE Rebholz2007The Swiss Childhood Cancer Registry: rationale, organisation and results for the years 2001–2005.Swiss Medical Weekly137502509
- 33. Feller M, Adam M, Zwahlen M, Brazzola P, Niggli F, et al. (2010) Family Characteristics as Risk Factors for Childhood Acute Lymphoblastic Leukemia: A Population-Based Case-Control Study. PLoS ONE 5: e13156.M. FellerM. AdamM. ZwahlenP. BrazzolaF. Niggli2010Family Characteristics as Risk Factors for Childhood Acute Lymphoblastic Leukemia: A Population-Based Case-Control Study.PLoS ONE5e13156
- 34. Robison LL, Mertens AC, Boice JD (2002) Study design and cohort characteristics of the Childhood Cancer Survivor Study: a multi-institutional collaborative project. Med Pediatr Oncol 38: 229–239.LL RobisonAC MertensJD Boice2002Study design and cohort characteristics of the Childhood Cancer Survivor Study: a multi-institutional collaborative project.Med Pediatr Oncol38229239
- 35. Hawkins M, Lancashire E, Winter D, Frobisher C, Reulen R, et al. (2008) The British Childhood Cancer Survivor Study: Objectives, methods, population structure, response rates and initial descriptive information. Pediatric Blood & Cancer 50: 1018–1025.M. HawkinsE. LancashireD. WinterC. FrobisherR. Reulen2008The British Childhood Cancer Survivor Study: Objectives, methods, population structure, response rates and initial descriptive information.Pediatric Blood & Cancer5010181025
- 36. Liebherr R, Marquis J, Storni M, Wiedenmayer G (2010) Gesundheit und Gesundheitsverhalten in der Schweiz 2007 - Schweizerische Gesundheitsbefragung. Neuchâtel: Bundesamt für Statistik. R. LiebherrJ. MarquisM. StorniG. Wiedenmayer2010Gesundheit und Gesundheitsverhalten in der Schweiz 2007 - Schweizerische GesundheitsbefragungNeuchâtelBundesamt für Statistik
- 37. Germann U (2005) Abschlussbericht zur Volkszählung 2000. Neuchâtel: Bundesamt für Statistik. U. Germann2005Abschlussbericht zur Volkszählung 2000NeuchâtelBundesamt für Statistik
- 38. Godin G, Jobin J, Bouillon J (1986) Assessement of leisure time exercise behavior by self-report: a concurrent validity study. Can J Public Health 77: 359–362.G. GodinJ. JobinJ. Bouillon1986Assessement of leisure time exercise behavior by self-report: a concurrent validity study.Can J Public Health77359362
- 39. Mäder U, Martin BW, Schutz Y, Marti B (2006) Validity of Four Short Physical Activity Questionnaires in Middle-Aged Persons. Medicine & Science in Sports & Exercise 38: 1255–1266.U. MäderBW MartinY. SchutzB. Marti2006Validity of Four Short Physical Activity Questionnaires in Middle-Aged Persons.Medicine & Science in Sports & Exercise3812551266
- 40. Kuehni CE, Strippoli MPF, Rueegg CS, Rebholz CE, Bergstraesser E, et al. (2012) Educational achievement in Swiss childhood cancer survivors compared with the general population. Cancer 118: 1439–1449.CE KuehniMPF StrippoliCS RueeggCE RebholzE. Bergstraesser2012Educational achievement in Swiss childhood cancer survivors compared with the general population.Cancer11814391449
- 41. World Health Organization (1995) Physical status: The use and interpretation of anthropometry. Geneva, Switzerland: World Health Organization. World Health Organization1995Physical status: The use and interpretation of anthropometryGeneva, SwitzerlandWorld Health Organization
- 42. Steliarova-Foucher E, Stiller C, Lacour B, Kaatsch P (2005) International Classification of Childhood Cancer, third edition. Cancer 103: 1457–1467.E. Steliarova-FoucherC. StillerB. LacourP. Kaatsch2005International Classification of Childhood Cancer, third edition.Cancer10314571467
- 43. Westerterp K (2009) Assessment of physical activity: a critical appraisal. European Journal of Applied Physiology 105: 823–828.K. Westerterp2009Assessment of physical activity: a critical appraisal.European Journal of Applied Physiology105823828
- 44. Wynder EL, Higgins IT, Harris RE (1990) The wish bias. Journal of Clinical Epidemiology 43: 619–621.EL WynderIT HigginsRE Harris1990The wish bias.Journal of Clinical Epidemiology43619621
- 45. Mäkinen T, Kestilä L, Borodulin K, Martelin T, Rahkonen O, et al. (2010) Effects of childhood socio-economic conditions on educational differences in leisure-time physical activity. The European Journal of Public Health 20: 346–353.T. MäkinenL. KestiläK. BorodulinT. MartelinO. Rahkonen2010Effects of childhood socio-economic conditions on educational differences in leisure-time physical activity.The European Journal of Public Health20346353
- 46. Ness KK, Hudson MM, Ginsberg JP, Nagarajan R, Kaste SC, et al. (2009) Physical Performance Limitations in the Childhood Cancer Survivor Study Cohort. Journal of Clinical Oncology 27: 2382–2389.KK NessMM HudsonJP GinsbergR. NagarajanSC Kaste2009Physical Performance Limitations in the Childhood Cancer Survivor Study Cohort.Journal of Clinical Oncology2723822389
- 47. Thornton J (1997) Overcoming the protected child syndrome: Kids, exercise and chronic illness. Physician Sportsmed 25: 97–100.J. Thornton1997Overcoming the protected child syndrome: Kids, exercise and chronic illness.Physician Sportsmed2597100
- 48. San Juan AF, Chamorro-Viña C, Moral S, Fernández del Valle M, Madero L, et al. (2008) Benefits of Intrahospital Exercise Training after Pediatric Bone Marrow Transplantation. Int J Sports Med 29: 439–446.AF San JuanC. Chamorro-ViñaS. MoralM. Fernández del ValleL. Madero2008Benefits of Intrahospital Exercise Training after Pediatric Bone Marrow Transplantation.Int J Sports Med29439446
- 49. Barr-Anderson DJ, AuYoung M, Whitt-Glover MC, Glenn BA, Yancey AK (2011) Integration of Short Bouts of Physical Activity Into Organizational Routine: A Systematic Review of the Literature. American Journal of Preventive Medicine 40: 76–93.DJ Barr-AndersonM. AuYoungMC Whitt-GloverBA GlennAK Yancey2011Integration of Short Bouts of Physical Activity Into Organizational Routine: A Systematic Review of the Literature.American Journal of Preventive Medicine407693
- 50. US Department of Health and Human Services (2000) Healthy people 2010. Washington, DC: Government Printing Office. US Department of Health and Human Services2000Healthy people 2010Washington, DCGovernment Printing Office
- 51. US Department of Health and Human Services (1996) Physical Activity and Health: A Report of the Surgeon General. Washington, DC: US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion. US Department of Health and Human Services1996Physical Activity and Health: A Report of the Surgeon GeneralWashington, DCUS Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion
- 52. Winter C, Müller C, Hoffmann C, Boos J, Rosenbaum D (2009) Physical activity and childhood cancer. Pediatric Blood & Cancer 54: 501–510.C. WinterC. MüllerC. HoffmannJ. BoosD. Rosenbaum2009Physical activity and childhood cancer.Pediatric Blood & Cancer54501510
- 53. Oeffinger K, Hudson MM (2004) Long term complications following childhood and adolescent cancer: foundations for providing the risk based health care for survivors. CA Cancer J Clin 54: 208–236.K. OeffingerMM Hudson2004Long term complications following childhood and adolescent cancer: foundations for providing the risk based health care for survivors.CA Cancer J Clin54208236
- 54. Butterfield RM, Park ER, Puleo E, Mertens A, Gritz ER, et al. (2004) Multiple risk behaviors among smokers in the childhood cancer survivors study cohort. Psycho-Oncology 13: 619–629.RM ButterfieldER ParkE. PuleoA. MertensER Gritz2004Multiple risk behaviors among smokers in the childhood cancer survivors study cohort.Psycho-Oncology13619629