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Medical Screening Participation in the Childhood Cancer Survivor Study
Cheryl L. Cox, PhD;
Melissa M. Hudson, MD;
Ann Mertens, PhD;
Kevin Oeffinger, MD;
John Whitton, MS;
Michele Montgomery, MPH;
Leslie L. Robison, PhD
Arch Intern Med. 2009;169(5):454-462.
ABSTRACT
Background Despite their risk for serious late sequelae, survivors of childhood cancer do not adhere to recommended medical screening guidelines. We identified treatment, survivor, physician, and contextual factors that may influence survivor adherence to recommended echocardiography and bone densitometry screening.
Methods Structural equation modeling of data from the Childhood Cancer Survivor Study; 838 participants had received a diagnosis of and were treated for pediatric cancers between 1970 and 1986.
Results Survivors at risk of cardiac sequelae (n = 316; mean [SD] age, 31.01 [7.40] years; age at diagnosis, 9.88 [5.88] years; and time since diagnosis, 21.14 [4.37] years) who reported more cancer-related visits (P = .01), having discussed heart disease with a physician (P  .001), with a sedentary lifestyle (P = .05), and less frequent health fears (P = .05) were most likely to follow the recommended echocardiogram schedule (R2 = 23%). Survivors at risk of osteoporosis (n = 324; age, 30.20 [7.09] years; age at diagnosis, 9 .01 [5.51]years; and time since diagnosis, 21.20 [4.27] years) who reported more cancer-related visits (P = .05), were followed up at an oncology clinic (P = .01), had discussed osteoporosis with a physician (P .001), and had a lower body mass index (P = .05) were most likely to adhere to the recommended bone density screening guidelines (R2 = 26%). Symptoms and motivation influenced screening frequency in both models.
Conclusions Multiple factors influence survivor adherence to screening recommendations. It is likely that tailored interventions would be more successful in encouraging recommended screening in survivors of childhood cancer than would traditional health education approaches.
INTRODUCTION
Improvement in the rates of childhood cancer survival has prompted greater awareness of late treatment-related morbidity. Among the potential sequelae of therapy are osteoporosis, cardiomyopathy, and secondary neoplasms.1-4 The Children's Oncology Group has compiled risk-based, exposure-related clinical practice guidelines for screening and management of late effects resulting from treatment of pediatric cancers.5 A baseline echocardiographic screening is recommended for survivors at entry to long-term follow-up and then periodically based on age at treatment, radiation dosage, and cumulative anthracycline dosage (Table 1). Survivors who are at highest risk and, therefore, should undergo more frequent screening are those who were younger than 5 years at treatment and who received any anthracycline therapy or who had any radiation exposure. Baseline dual-energy x-ray absorptiometry screening for bone density is recommended at entry to long-term follow-up and is repeated as clinically indicated (Table 1). While exposure-based guidelines for screening for the late effects of pediatric cancer treatment have been established, survivor medical screening practices are suboptimal.6-8
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Table 1. Treatment Exposure and Screening Guidelinesa
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The medical screening literature limited to survivors of childhood cancer is confined to breast and cervical cancer8-9 and cardiovascular disease.9 Of women in the Childhood Cancer Survivor Study (CCSS) (n = 12 101), 78.2% reported undergoing a Papanicolaou test within the previous 3 years, 62.4% underwent a clinical breast examination within the last year, and 20.9% had undergone mammography at least once in their lifetime.8 Survivors of childhood cancer who received chest irradiation are at increased risk of developing breast cancer before age 40 years.10-12 A prospective study of survivors of Hodgkin disease found that only 41 of 87 (47%) reported having undergone mammography in the previous 24 months; only 417 of 852 female survivors (49%) at increased risk of breast cancer underwent mammography within the previous 24 months.9 Treatment of childhood cancer with anthracyclines, radiation, or both increases the risk of late cardiotoxic effects.4, 13-15 However, only 503 of 1798 (28%) survivors of childhood cancer at increased risk of cardiac disease underwent the recommended cardiac screening in the previous 24 months.9
In addition to disease and treatment factors, personal and contextual factors influence health behavior choices.16-21 To describe the multiple influences on survivor screening behaviors, we selected the Interaction Model of Client Health Behavior,22-23 which incorporates both intrapersonal and contextual variables and has been adapted to the study of survivors of childhood cancer (Figure 1). Structural equation modeling (SEM), which combines factor and path analyses in a comprehensive method,24 enabled us to test the model's hypotheses simultaneously rather than sequentially. Our goal was to identify treatment, survivor, physician, and contextual factors that could be targeted with behavioral interventions to support recommended screening.
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Figure 1. Correspondence of the Interaction Model of Client Health Behavior with study variables.
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METHODS
DATA SOURCE
The CCSS is a multi-institutional retrospective cohort study initiated in 1994 to examine the late effects of pediatric cancer diagnosed and treated between 1970 and 1986. Survivors completed a baseline questionnaire at study enrollment and respond to follow-up questionnaires sent at regular intervals. Questionnaires and sampling methods are detailed by Robison et al25 and are available for review at http://www.stjude.org/ccss. The study was approved by the institutional review board of St Jude Children's Research Hospital, Memphis, Tennessee.
SAMPLE
Originally, 20 346 survivors were contacted to participate in the CCSS. Eligible participants had survived 5 years or longer after being treated for a malignant disease diagnosed (before the age of 21 years) between January 1, 1970, and December 31, 1986; approximately 12 423 were alive at the time of analysis. An ancillary study, the Health Care Needs Survey (HCNS), initiated by one of us (K.O.), randomly sampled 1600 of the survivors. Of the 978 participants (61%) who completed and returned the survey, 838 (86%) returned the second follow-up survey of the CCSS within the same data collection period. Nonrespondents to the HCNS were typically men (59%), members of racial/ethnic minority groups (37%), or had achieved an educational level of less than high school (56%). Survivors who completed the HCNS but not the second follow-up survey were younger at diagnosis (P = .02) and had received the diagnosis more recently (P = <.001). No survivor reported herein was younger than 18 years at the time of self-reported data collection (Table 2).
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Table 2. Descriptive Summary of the Total Sample and At-Risk Groupsa
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Respondents to the CCSS self-identified their race/ethnicity (white, black, American Indian or Alaskan Native, Asian or Pacific Islander, Hispanic, and other) on the basis of structured response categories used in the baseline questionnaire. The analyses in this article were restricted to survivors classified as white, black, Hispanic, and other because there were too few respondents in the other categories to enable meaningful analyses.
We selected and modeled 2 at-risk subsamples on the basis of treatment exposures (Table 1) who had responded to the baseline, HCNS, and second follow-up surveys: a cardiac risk group (exposure to anthracycline or irradiation or both) and a bone density risk group (cranial radiotherapy and glucocorticoid, methotrexate, or prolonged corticosteroid therapy).
OUTCOME MEASURES
Single items addressed the time since the last echocardiographic or bone densitometry evaluation (1 indicates never; 2,  5 years; 3, >2 years but <5 years; 4, 1-2 years; and 5, <1 year) (Table 3). Survivors who answered "Don't know" for time since any of the screening examinations were excluded from the analysis.
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Table 3. Summary of Study Measuresa
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INDEPENDENT MEASURES
Two types of variables are modeled in SEM: observed and latent. In contrast to observed variables that can be directly measured (eg, test scores), latent variables (eg, depression) are measured indirectly by a set of observed variables.26 Our final models have 10 directly observed measures and 4 latent measures (Figure 2) that contributed directly, indirectly, or jointly to the explained variance in frequency of echocardiography or bone densitometry.
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Figure 2. Predictors of echocardiographic (A) and bone densitometry (B) screening. A nonsignificant  2 test statistic measures the absolute fit of the model to the data but is insensitive to sample size.27 The Comparative Fit Index (CFI) and Tucker-Lewis Index (TLI) test the proportionate improvement in fit by comparing the target model with an independent base model; a value of 0.90 is minimally acceptable,28 values approximating 0.95 indicate a good fit, and values at or close to 1.00 indicate an excellent fit.29 The root mean square of approximation (RMSEA) represents closeness of fit, and values approximating 0.06 and 0.00 demonstrate close and exact fit of the model, respectively.29-30 CI indicates confidence interval; Prob, probability; rectangles, directly observed measures; ovals, latent measures.
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Directly Observed Independent Variables
Although all variables corresponding to the conceptual model were examined as potential covariates, the following directly observed independent variables were statistically significant in the final models: (1) survivor pain resulting from cancer or its treatment (1 indicates no pain; 5, excruciating pain); (2) number of cancer-related visits in the last 2 years (1, none; 7, >20); (3) survivor perception of the severity of late effects (1, moderate, severe, or life-threatening; 2, mild or no chronic problems); (4) physician-survivor discussion of osteoporosis (1, yes; 2, no); (5) physician-survivor discussion of heart disease (1, yes; 2, no); (6) follow-up at an oncology clinic in the last 2 years (1, yes; 2, no); (7) receipt of a print media intervention detailing exposure risks and recommended follow-up for cardiac or bone density sequelae (1, yes; 0, no); (8) baseline aerobic exercise frequency (sweat or breathe hard for 20 minutes on 0-7 days); (9) physically active leisure-time lifestyle during the last month (1, yes; 2, no); and (10) level of readiness for medical follow-up (1, precontemplation; 2, contemplation; and 3, action).
Latent Independent Variables
The following latent independent variables were significant in the final models: (1) fear or worry: 3 observed variables including survivor worry about future health, recurrence of cancer, and fear that a problem will be discovered at a check-up visit (1 indicates moderate, quite a bit, or extremely concerned; 2, not at all or a little concerned) ( = .76); (2) health concerns: 3 observed variables including survivor general concerns about health, concerns about chance of getting sick, and perception about the importance of a check-up visit (1 indicates moderate, quite a bit, or extremely concerned; 2, not at all or a little concerned) ( = .79); (3) intrinsic motivation: 5 observed items from the Multidimensional Health Locus of Control Scale,31 for example, "I am in control of my health" (1, strongly disagree; 6, strongly agree) ( = .79); (4) extrinsic motivation: 5 items from the Multidimensional Health Locus of Control Scale,31 for example, "Health professionals control my health" (1, strongly disagree; 6, strongly agree) ( = .80).
STATISTICAL ANALYSES
SEM has 2 components: the measurement model evaluates whether observed measures (eg, scales or self-reports) adequately represent the latent variables, and model hypotheses (Figure 1) are then tested for the interrelation of the latent variables and covariates.32 SEM was performed with Mplus version 4.2 (Muthén & Muthén, Los Angeles, California).26 The models are based on subjects with complete data; sample sizes for each model were more than adequate.33
Multiple indicators assess how the SEM fit the data27-30 (Figure 2). Factor loading values for the latent variables were less than or equal to P = .01 across both models and factor score determinacy values were greater than or equal to 0.80, which suggests that measures of the latent constructs were strong. The final models have significant parameter estimates (Appendix available on request from the author) corresponding to the hypothesized relationships, meet the established SEM fit criteria (Figure 2), and offer the highest percentage of explained variance for the outcome.
RESULTS
The typical respondent was a white, unmarried, female college graduate with a personal annual income of $19 999 to $39 999; she had health insurance and had not been seen at an oncology clinic in the last 2 years (Table 2). Compared with the total sample, participants in the risk groups had received a diagnosis more recently (not significant with Bonferroni adjustment for multiple comparisons, P = .02), had a slightly higher educational achievement level, and were more likely to have been followed up recently in an oncology clinic. At diagnosis, the cardiac risk group was slightly older than the bone density risk group (Table 2). In the cardiac risk group, 42.1% of participants had never undergone echocardiography or had not within the last 5 years; however, those at cardiac risk were more likely to have undergone echocardiography more recently (2-4 years) than either the total sample or the bone density risk group. Nearly 75% of those in the bone density risk group had never undergone bone densitometry or had not within the last 5 years, and they were no more likely than the cardiac risk group to have undergone bone densitometry at the recommended intervals (Table 3).
Survivors at cardiac risk were more likely than the total sample and those in the bone density risk group to have discussed heart disease with their physician and to be at least 40 years of age. Survivors in the total sample were more likely to have received a print media intervention detailing their treatment risks; however, a greater percentage of those in the bone density risk group received the intervention compared with those in the cardiac risk group (Table 3).
FREQUENCY OF ECHOCARDIOGRAPHY
A strong model explained 23% of the variance in the recency of undergoing echocardiography in survivors most at risk of cardiac sequelae (Figure 2A). Survivors who were most likely to follow a more frequent echocardiogram schedule reported more cancer-related visits, discussion of heart disease with a physician, a sedentary lifestyle, and less frequent health fears. The number of cancer-related visits was predicted by reports of increased pain, lower levels of aerobic exercise at baseline, increased readiness for medical follow-up, and perception of more severe late effects. Less frequent health fears predicted an active lifestyle. More cancer pain, higher levels of extrinsic motivation, and perception of more severe late effects predicted more frequent health fears. Increased readiness to seek medical follow-up was predicted by increased extrinsic motivation, frequent health fears, and more severe late effects. Significant positive indirect effects on the recency of undergoing echocardiography included cancer-related pain (P = .01) and increased readiness for medical follow-up (P = .05) through cancer-related visits.
FREQUENCY OF BONE DENSITOMETRY
A well-fitting bone densitometry model described participants who were adherent to the bone density screening guidelines (R2 = 26%) as having made more cancer-related visits, received follow-up at an oncology clinic, were more extrinsically motivated, had discussed osteoporosis with a physician, and had a lower body mass index. More health concerns, more cancer-related visits, and having received a print media intervention detailing the individualized risk of sequelae predicted recent oncology clinic follow-up (Figure 2B). Health concerns were predicted by more frequent health fears and reported higher extrinsic motivation. Greater health concerns, decreased intrinsic motivation, more cancer-related pain, perception of more severe late effects, and more frequent fatigue predicted increased fear about future health. More cancer-related visits predicted having discussed osteoporosis with a physician. More cancer-related visits and increased concerns about health indirectly predicted bone densitometry frequency through follow-up at an oncology clinic.
COMMENT
Adult survivors of childhood cancer at high risk frequently do not adhere to recommended medical screening guidelines. Most survivors reported having never discussed heart disease or osteoporosis with their physician. Survivors were most likely to adhere to recommended echocardiographic and bone densitometry screening schedules if they reported more frequent cancer-related visits or were followed up at an oncology clinic, or both. The extent to which our findings reflect the increase in sequelae of treatment, increase in confidence in the knowledge of the specialty provider, familiarity with the facility and its staff by those who had received more recent treatment, or more targeted delivery of care compared with that available in a nonspecialty facility requires further study. Only 7% of the study sample were followed up by a cancer specialist; only 4% were followed up at a cancer center. Because most survivors are not followed up in specialty clinics, this finding is particularly relevant for primary care physicians, who often lack knowledge about the unique health risks inherent in the treatment of childhood cancer.7, 34-37 Chronic health conditions in survivors of childhood cancer become more prevalent with increasing intervals since cancer treatment and are exacerbated by comorbid illnesses associated with aging and maladaptive health behaviors.38 Because specific treatment and survivor factors are linked to adverse health outcomes in survivors of childhood cancer, informed physician and allied health professional intervention based on risk-stratified medical surveillance represents an important opportunity to reduce cancer-related morbidity.
Pain, fatigue, and perception of severity of late effects were strong exogenous variables (unaffected by other variables) in both models. They were antecedent to increased health concerns, more frequent health fears, and a negative affect, which in turn directly or indirectly affected screening frequency. Pain is a frequently reported late effect39-40; 22.3% of 9034 survivors of childhood cancer reported having moderate to severe pain, and 14.3% reported pain sufficient to interfere with daily activities.41 Nineteen percent of 264542 and 30% of 161 adult survivors of childhood cancer reported fatigue.43 Fatigue and pain negatively affect quality of life43 and health behaviors that have the potential to modify late effects.44-45
More frequent health fears were a deterrent to undergoing echocardiography; however, more frequent fear also increased health concerns, which predicted more recent follow-up at an oncology clinic. Fear, worry, and anxiety exert both positive and negative influence on health-related behaviors.18, 46 Although early detection through medical screening may positively modify a disease course, the prospect of learning that one has a serious health condition can be profoundly frightening.47-48 Survivors may resort to avoidance behavior46 (eg, not going for routine screenings) to reduce fear, anxiety, and a negative affect or, in contrast, use screening as a means (eg, negative findings at screening examinations) to reduce the discomfort of fear and anxiety.27
Lack of specific information about risk factors and misconceptions can exacerbate fear or contribute to the denial of the existence of important health problems.49-51 Discussing late effects (eg, heart disease or osteoporosis) with a physician predicted more recent screening in both models. In the general population, specific physician recommendation is associated with a higher rate of screening for cervical,52 breast,53-54 prostate,54 colorectal,55-57 and skin58 cancers. More recent oncology clinic follow-up was predicted by survivor receipt of an individualized print media intervention that detailed treatment exposure risks for bone density–related late effects and recommendations for follow-up. The effect of the print media intervention on the bone density risk group may reflect that a larger percentage of this group received the intervention; in addition, this group may have had greater sensitivity or receptivity because of discernible symptoms (eg, pain or physical dysfunction).
Motivation had a prominent role in all of the models. Extrinsically motivated individuals are more worried and fearful about their health, think they are less able to exert control over health concerns, and are more likely to rely on health professionals for direction17, 23, 59; intrinsically motivated individuals are more self-reliant and self-directed rather than physician directed17, 60 in their health care choices. Because they may not have accurate health and risk information and have infrequent contact with a physician, intrinsically motivated survivors may be at greater risk of not adhering to screening guidelines. The complex interactions among fear, the patient-physician relationship, affect, and intrinsic motivation should be further explored.
The unique contributions of baseline exercise frequency and sedentary lifestyle to the echocardiogram model may reflect survivors who have early symptoms of treatment-related cardiac sequelae.45 Similarly, survivors with a low body mass index were more likely to adhere to bone densitometry recommendations.
LIMITATIONS OF THE STUDY
The study sample reflects a subset of the overall CCSS population, that is, those who responded to the HCNS and second CCSS follow-up survey; therefore, survivors included in the present analysis may not be fully representative of the population from which they were derived. The information used to classify the health screening outcomes, as well as the independent measures, were based on self-reported data. While the CCSS population represents a large and heterogeneous cohort of 5-year survivors, results may not be generalizable to all survivors of childhood cancer. As a group, CCSS participants may be more informed about risks and health promotion because of newsletters received as a result of participation in the study.
CLINICAL IMPLICATIONS
Primary care physicians are encouraged to specifically inquire about treatment-related symptoms, in particular, pain, fatigue, and anxiety.1, 43, 61 These symptoms may share common biological mechanisms62-64 and, until addressed, obstruct positive health behaviors. Physicians should elicit survivor concerns and address any misconceptions that may contribute to survivor lack of understanding about the importance of their risk of late effects. Therapeutically increasing or decreasing fear arousal65-66 by providing personalized information about the risk of late effects and the benefits of medical screening may enhance screening behavior. Focused interactions with survivors are important to reduce anxiety, support motivation, and contribute to a more positive affect, which in turn support adherence to screening recommendations.
CONCLUSIONS
Multiple factors can influence survivor adherence to screening recommendations, including already established sequelae (eg, pain, fatigue, and functional decline). Early interventions (before completion of therapy and during early posttherapy follow-up) that consider the multiple influences on survivor medical screening behaviors may be instrumental in modifying sequelae and supporting earlier screening. Providing the survivor of childhood cancer with written summaries of pediatric cancer therapy together with recommendations for screening and follow-up that can be shared with the primary care physician may be a useful adjunct for targeting increased medical screening.
AUTHOR INFORMATION
Correspondence: Cheryl L. Cox, PhD, Department of Epidemiology and Cancer Control, St Jude Children's Research Hospital, 332 N Lauderdale St, Memphis, TN 38105-2794 (cheryl.cox{at}stjude.org).
Accepted for Publication: September 2, 2008.
Author Contributions: Dr Cox had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Cox, Mertens, Oeffinger, and Montgomery. Acquisition of data: Mertens, Whitton, and Robison. Analysis and interpretation of data: Cox, Hudson, Oeffinger, and Whitton. Drafting of the manuscript: Cox, Montgomery, and Robison. Critical revision of the manuscript for important intellectual content: Cox, Hudson, Mertens, Oeffinger, Whitton, and Robison. Statistical analysis: Cox and Whitton. Obtained funding: Cox, Mertens, Oeffinger, and Robison. Administrative, technical, and material support: Cox, Hudson, Mertens, Whitton, Montgomery, and Robison. Study supervision: Cox and Robison.
Financial Disclosure: None reported.
Funding/Support: This study was supported by grants RO3 NR009203 (Dr Cox, principal investigator) and U24 CA55727 (Dr Robison, principal investigator) from the US Public Health Service, a grant from the Robert Wood Johnson Foundation, and support to St Jude Children's Research Hospital from the American Lebanese Syrian Associated Charities.
Previous Presentation: This study was presented as an abstract at the 136th Annual Meeting of the American Public Health Association; October 27, 2008; San Diego, California.
Additional Contributions: Sharon Naron, MPA, ELS, and Vani Shanker, PhD, provided editorial assistance, and Kelly Shempert provided the illustrations.
Author Affiliations: Department of Epidemiology and Cancer Control, St Jude Children's Research Hospital, Memphis, Tennessee (Drs Cox, Hudson, and Robison and Ms Montgomery); Department of Pediatrics, Emory University, Atlanta, Georgia (Dr Mertens); Department of Pediatrics, Memorial Sloan-Kettering Cancer Center, New York, New York (Dr Oeffinger); and Fred Hutchinson Cancer Research Center, Seattle, Washington (Mr Whitton).
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