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Journal of Clinical Oncology, Vol 25, No 15 (May 20), 2007: pp. 2100-2106 Published by the American Society of Clinical Oncology DOI: 10.1200/JCO.2006.06.6340 Provider Counseling About Health Behaviors Among Cancer Survivors in the United States
From the Division of Cancer Prevention and Control, National Centers for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, GA Address reprint requests to Susan A. Sabatino, MD, Centers for Disease Control and Prevention, Division of Cancer Prevention and Control, 4770 Buford Highway (K-52), Atlanta, GA 30341; e-mail: ssabatino{at}cdc.gov
Purpose To examine provider discussion or counseling of US cancer survivors about diet, exercise, and tobacco use. Methods We used 2000 National Health Interview Survey data to examine whether US cancer survivors reported that, within 1 year, a provider (1) discussed diet, (2) recommended they begin or continue exercise, or (3) asked about smoking. We included survivors more than 1 year beyond diagnosis (n = 1,600) and adults without cancer (AWCs; n = 24,636) who saw/talked to a provider within 1 year. We used generalized linear contrasts in bivariable analyses and logistic regression to calculate predicted marginals adjusted for age, sex, comorbidity, usual source of care, and number of provider visits in the prior year. Results Few survivors reported discussions or recommendations for all three health behaviors (10% of survivors v 9% of AWCs; P = .57). Although report was more likely than among AWCs, few survivors reported diet discussions (30% of survivors v 23% of AWCs; P < .0001) or exercise recommendations (26% of survivors v 23% of AWCs; P < .005), and a minority were asked about smoking (42% of survivors v 41% of AWCs; P = .41). After adjustment, survivors were less likely to report exercise recommendations than were AWCs (22% v 24%, respectively; P = .02). Colorectal cancer survivors were less likely than were AWCs of similar age range to report exercise recommendations (16% v 27%, respectively; P < .003) or smoking discussions (31% v 41%, respectively; P < .05). Cervical cancer survivors were more likely than AWCs of similar age range to discuss smoking (58% v 43%, respectively; P < .001). Conclusion Findings from this nationally representative sample suggest that many providers may miss opportunities to counsel survivors about healthy behaviors, perhaps particularly colorectal cancer survivors.
Cancer survivors include individuals along the spectrum between receiving a cancer diagnosis through the remainder of life and family, friends, and caregivers of people diagnosed with cancer.1 In this article, "cancer survivors" include people with a cancer history, a growing segment of the population.2 Cancer risk increases with age, and the population is aging. The development of more effective screening and diagnostic tests has improved clinicians' ability to detect cancers and to detect them earlier.3 Furthermore, 5-year survival rates are high for many cancers.2,4 Estimates suggest that 64% of cancer patients survive beyond 5 years2 and that more than 10 million people currently living in the United States are survivors.5 An increasing emphasis has been placed on addressing the needs of this population.1 The recent Institute of Medicine (IOM) report on cancer survivorship expressed concerns that cancer survivors are becoming lost to follow-up after treatment, and are failing to fully appreciate their increased health risks.6 Coordinated care plans are deemed "essential so that routine follow-up visits become opportunities to promote a healthy lifestyle."6 Research suggests that obesity, physical inactivity, or tobacco use increase cancer risk,7-9 and may be related to second cancers,6 treatment complications,6,10 quality of life,6,11 and survival.6,12 Health behaviors also likely affect other conditions for which cancer survivors may have increased risk, such as cardiovascular disease,13,14 diabetes,15 osteoporosis,16 and psychosocial problems.13,17 A recent study of behavioral risk factors using nationally representative data concluded several risk factors were common among survivors, including inactivity (59% to 79%), being overweight (52% to 68%), poor diet (45% to 50%), and tobacco use (8% to 38%).18 Little is known about the extent to which health care providers address these issues with survivors. Despite evidence of effectiveness for some interventions,3 previous studies in the general population suggest providers may not counsel many patients about lifestyle, with 25% to 42% of individuals reporting recent dietary or exercise advice from a provider.19-21 Interventions promoting dietary changes, exercise, and smoking cessation6,22-24 suggest that survivors may be responsive to such efforts. Evaluating counseling of survivors about health behaviors will help delineate current practices and target potential areas for intervention. We examined rates of provider discussion or counseling of US cancer survivors about diet, exercise, and tobacco use. We included comparison groups of adults without cancer because the literature suggests that health-related behavior counseling in the general population is low. Given this, we anticipated that rates in both populations would be low. The general population rates provide a benchmark in considering rates among survivors. Although IOM and other recommendations were published after 2000, we anticipated that counseling might be higher among survivors, given their health risks.
We used data from the 2000 National Health Interview Survey,25 a nationally representative sample of the civilian, noninstitutionalized US population. The National Health Interview Survey is an annual survey administered by the National Center for Health Statistics through in-person interviews. We used the Sample Adult Core (response rate, 72%), for which one adult per household was randomly selected to provide information. We identified 26,402 adults who saw or talked to a health care provider within the prior year. We excluded 23 respondents with unknown cancer history. Of those remaining, 1,743 reported a cancer history other than nonmelanoma skin cancer. We excluded 143 adults diagnosed with cancer in the prior year because we were unable to determine whether they had been counseled before or after diagnosis. Our sample included 1,600 cancer survivors and 24,636 adults without cancer or nonmelanoma skin cancer history only (AWCs). We also examined the frequency of counseling for subgroups of the most commonly reported cancers (Table 1), classified by first diagnosis. For each cancer subgroup, we defined a corresponding AWC subgroup no younger than the youngest survivor in that cancer subgroup, to limit age differences between subgroups. For sex-specific cancers, the corresponding comparison group was limited to the same sex.
Our dependent variables included reports that, within the prior year, a health care provider "talked with you about your diet and eating habits," "recommend[ed] that you begin or continue to do any type of exercise or physical activity," or "asked you about whether you smoke cigarettes or use other kinds of tobacco." Current smokers were also asked if a provider advised them to quit. Providers included "doctor or other health professional."25
We considered several other factors shown to influence provider recommendations about health behavior in the literature, including age, sex, and comorbid illness.19,20,26,27 Comorbid illnesses (categorized as 0, 1, and 2+) included heart disease, stroke, hypertension, emphysema, chronic bronchitis, diabetes, liver disease, and weak/failing kidneys. We considered several additional factors likely to reflect opportunities to receive a recommendation via facilitated or more frequent provider contact, including having a usual source of care and number of provider visits in the prior year. Furthermore, we considered body mass index (BMI; < 19.0, 19.0 to 24.9, We used SUDAAN (RTI, Research Triangle Park, NC) to account for the complex sample design25 and weighted results to reflect national estimates. Weights are poststratified by age, sex, race and/or ethnicity classes on the basis of US Census controls.25 We used generalized linear contrasts in bivariable analyses, and logistic regression to estimate the adjusted percentages (predicted marginals) of counseling among survivors and AWCs. We fit separate models for each dependent variable for the entire sample and for each subgroup pair. All models were adjusted for age, sex, comorbid illnesses, usual source of care, and visit number. Because we were unable to determine whether BMI, exercise, and smoking behavior predated or possibly resulted from counseling, these factors were not initially included to avoid controlling for behaviors that may be a consequence of counseling. To adjust for possible differences in BMI or health-related behaviors before counseling, we adjusted diet models for BMI, exercise models for BMI and physical activity, and tobacco models for smoking status. Caution is needed in interpreting P values. We examined counseling on health behaviors among several groups of survivors and AWCs, raising the issue of multiple comparisons. Methodologists offer inconsistent recommendations on this issue.31 The Bonferroni correction would yield a significance level of P < .003; however, it can be overly conservative, and we are not aware of other methods of adjusting for multiple comparisons with binary data implemented in software for use with complex sample surveys. We intended to examine counseling on each behavior in each survivor group regardless of findings for other survivor groups and did not adjust for multiple comparisons; rather, we presented results with CIs31 for the reader's consideration.
Cancer survivors were older than AWCs (Table 2) and were more likely to be female, white, non-Hispanic, and former smokers; to exercise less than recommended; and to have low BMI, less than a college education, a usual source of care, more visits, and more comorbid illnesses. Some differences may be attributable in part to age differences between groups. Most survivors were overweight and exercised less than recommended, and 19% were current smokers.
Survivors (Table 1) were most likely to report breast and prostate cancers and less likely to report childhood cancers. Most were more than 5 years beyond diagnosis. Overall, 10% of cancer survivors and 9% of AWCs reported being asked or advised about all three behaviors (not shown). Before statistical adjustment (Table A1, Appendix, online only), survivors were more likely than were AWCs to report discussing diet (30% v 23%, respectively; P < .0001) or receiving an exercise recommendation (26% v 23%, respectively; P = .005). Colorectal cancer (CRC) survivors were less likely than their comparison group to report receiving exercise recommendations (18% v 26%, respectively; P = .04) or being asked about smoking (28% v 40%, respectively; P = .005). Uterine cancer survivors were more likely than were their comparison group to report discussing diet (37% v 24%, respectively; P = .02). Cervical cancer survivors were more likely than were their comparison group to report being asked about smoking (63% v 42%, respectively; P < .0001). Among survivors who were current smokers (n = 293), 63% (95% CI, 56.1% to 68.7%) reported advice to quit, compared with 52% (95% CI, 50.4% to 54.0%) of smokers without cancer (n = 5,067). After adjustment for age, sex, visit number, comorbid illnesses, and having a usual place of care, the difference between all cancer survivors and AWCs in diet counseling was eliminated, and the difference between uterine cancer survivors and their comparison group was not significant (Table 3). For exercise, the all-survivors group became significantly less likely, rather than more likely, than AWCs to report receiving recommendations. However, CRC survivors remained less likely than their comparison group to report receiving a recommendation. Cervical cancer survivors remained more likely and CRC survivors less likely than their comparison groups to report being asked about tobacco, although differences were attenuated.
When we further adjusted models for BMI, physical activity, or smoking status (not shown), findings were virtually unchanged for diet counseling among all survivors and AWCs, and each subgroup pair. For exercise, the all-survivors group remained less likely than AWC to report recommendations, although no longer significant (22% v 24%, respectively; P = .06). CRC survivors remained less likely than their comparison group to report exercise recommendations (16% v 27%, respectively; P = .003) and being asked about smoking (31% v 41%, respectively; P = .04). Cervical cancer survivors remained more likely than their comparison group to report being asked about smoking, although differences were weakened (52% v 43%, respectively; P = .05). No other substantial changes were observed. When we examined counseling among cancer survivors by time since diagnosis after adjusting for age (Table 4), counseling for diet and smoking decreased over time, although for smoking the difference was not significant. For exercise, survivors 6 to 10 years since diagnosis reported fewer recommendations than did survivors 3 to 5 years since diagnosis.
In this nationally representative sample of the United States, reported rates of provider counseling about diet, exercise, or tobacco were low regardless of cancer history, with very few respondents reporting counseling about all behaviors. Less than one third of cancer survivors reported counseling or recommendations about diet or exercise, although survivors were more likely than were AWCs to report counseling. However, compared with adults of similar age, sex, comorbidity, and provider contact, survivors were not more likely to receive dietary or exercise counseling, and remained as likely to be asked about tobacco. In fact, they were less likely to receive exercise recommendations, although differences were small. Both survivors and AWCs more commonly reported being asked about smoking than about other behaviors. However, less than half of survivors reported being asked about tobacco. This was true for each cancer subgroup except cervical cancer. Differences in BMI, physical activity, and smoking had little effect. Ascertaining cancer survivors' behavior regarding diet, exercise, and smoking is important because these behaviors may influence conditions for which survivors may be at risk.9,13-15,17 Furthermore, these behaviors may affect quality of life,9,11,32-34 symptoms or adverse effects,10,34,35 and psychosocial well-being.10,11,32-36 Moreover, survivors may be interested in receiving information about these behaviors from providers,9,37 and many may be appropriate for counseling. Consistent with previous evidence,13,18,23,36,38,39 health-related lifestyle risk factors were common among survivors in our study, with only one quarter achieving recommended activity levels, most overweight or obese, and almost 20% currently smoking. Findings regarding exercise and diet are consistent with the literature.24,32,40 A recent review suggests almost 70% of breast cancer survivors reported receiving little or no information about exercise from providers, and 50% reported not receiving an exercise recommendation during treatment.32 Others found that 35% of early-stage breast and prostate cancer survivors reported a physician recommendation to exercise during cancer care,40 and that 19% of survivors reported a recommendation to change exercise.24 Although outcomes vary somewhat across studies, findings seem to suggest that few cancer survivors receive exercise counseling from providers. Evidence also suggests that fewer than one third of survivors reported physician recommendations about diet,24,40 consistent with our findings. Most cancer survivors who smoke reported a recommendation to quit (63%), similar to other estimates (67% to 74%).24,40,41 However, more than one third did not report receiving such advice. Being asked about smoking was more commonly reported than were discussions about other health behaviors, as in previous studies.20,24 However, despite the adverse health outcomes of smoking,7 the known effectiveness of tobacco counseling in the general population,3,42 recommendations by the US Preventive Services Task Force (USPSTF) that providers promote smoking assessment for all adults,3 and suggested methods for counseling about smoking cessation,3,43 most survivors did not report being asked about smoking. This could be due in part to the known nonsmoker status of some survivors, although some guidelines recommend that all patients should be asked about tobacco use and have their status documented regularly.44 One exception was among cervical cancer survivors, perhaps because of the known causal role of smoking in cervical cancer.7 Despite higher rates of assessing smoking among survivors compared with diet or exercise, opportunity exists to further improve assessment rates. Our findings suggest that health behavior counseling about exercise and smoking may be less likely among CRC survivors than among AWCs. This was not explained by differences in age, sex, comorbid illnesses, provider contact, or health behaviors. The less frequent inclusion of CRC survivors in health-related lifestyle intervention studies9 may contribute to less counseling about these behaviors. However, other survivors have been infrequently included in these intervention studies (eg, cervical cancer survivors); however, we did not observe lower counseling for them in our study. Furthermore, guidelines for follow-up of CRC patients available during the study period focused on detecting recurrence rather than modifying health behaviors.45,46 However, guidelines for other survivors had a similar focus.47 Confirmation of these findings and identification of determinants are needed. Our study contributes important information to the limited body of literature regarding health behavior assessment among cancer survivors, before recent recommendations. Several organizations comment on the management of health behaviors among survivors. The American Cancer Society states that "achieving and maintaining a healthy weight with appropriate diet and physical activity" is important for survivors, and provides general guidance for survivors about diet, exercise, and weight.48 The National Cancer Institute comments that survivors' "eating practices ... should be assessed throughout the continuum of care"49; and the President's Cancer Panel recommends that, on termination of treatment, survivors should receive "specific recommendations for healthy behaviors (eg, diet, exercise, sunscreen use, virus protection, smoking cessation)."50 Moreover, the USPSTF strongly recommends that clinicians screen all adults about smoking.3 Although some organizations conclude that exercise is generally safe34 or likely beneficial for most survivors,48 questions about safety for some may remain.6,9,32,34 This could explain, in part, the low rates of exercise recommendation among survivors in our study, although differences compared with AWCs were small. Other factors that may have contributed to low rates among survivors include lack of provider awareness of potential benefits of a healthy lifestyle, diffusion of responsibility among providers, lack of guidelines for long-term survivor follow-up, lack of reimbursement, or lack of office systems to promote health behavior assessment and counseling. Cancer survivors may also have more clinical issues than do AWCs, yielding increased competing demands during visits that may pre-empt health behavior counseling. We have controlled for this to some extent by only including survivors 1 year or more beyond diagnosis and therefore likely beyond active treatment, and by adjusting for comorbid illnesses. In addition, with few exceptions, counseling was not significantly lower among survivors than among AWCs, as would have been expected. Uncertainty about the effectiveness of counseling and somewhat inconsistent recommendations may also deter some providers from addressing these behaviors, even in the general population. Brief interventions for smoking cessation3 and intensive dietary counseling for adults at risk for diet-related chronic diseases3 are effective. Assessing current behavior is an important first step to identify those who may benefit. Although the USPSTF acknowledges the health benefits of exercise, it found insufficient evidence to recommend for or against exercise counseling, given uncertainty about duration of effect.3 Other organizations recommend providers counsel about physical activity,29,48,51 and Healthy People 2010 has objectives for increasing counseling about diet, exercise, and tobacco in the general population.29 Less information is available about the effectiveness of counseling among cancer survivors,6,52 although preliminary evidence may suggest that some counseling may have an effect. According to the IOM, interventions to promote smoking cessation among survivors are generally associated with high quit rates, although relapses may be common and sustained or repeated efforts may be needed.6 Tobacco education and counseling may also be associated with reduced smoking intentions in some survivors.53 In addition, exercise recommendations from oncologists may increase physical activity among newly diagnosed breast cancer survivors.23 However, among survivors of various cancers, many 1 year or more beyond diagnosis, physician recommendation to change exercise was not significantly associated with behavior change, although it neared significance (95% CI, 0.97 to 3.57). Physician recommendation was associated with healthful dietary changes.24 Our findings should be interpreted in light of several limitations. Data are self-reported. We do not have corroborative information about whether counseling was actually provided. Additionally, data are cross-sectional. Evaluation with longitudinal data is needed to determine temporal relationships between cancer diagnosis and health behavior counseling. Furthermore, some residual confounding by age or other factors may exist, and we did not have stage or treatment information, which could influence counseling decisions. As discussed in Methods, we examined counseling on health behaviors among several groups of survivors and AWCs, raising the issue of multiple comparisons, and the optimal method to address this issue is uncertain.31 Some statistically significant findings did not meet the more conservative Bonferroni corrected significance level. Although whether counseling is significantly different among cancer survivors than among AWCs may need further confirmation in these cases, the low counseling rates observed for survivors are consistent with previous literature, as noted herein. Moreover, some findings are plausible on the basis of literature or internal consistency within our study (eg, the lower counseling rates about both exercise and smoking among CRC survivors). These findings need confirmation. In summary, reported health behavior counseling rates are notably low among cancer survivors, as for AWCs. Clinical visits with survivors may represent "teachable moments" to encourage more healthful lifestyle choices.6,9 However, our findings suggest many providers may miss opportunities to counsel survivors about these behaviors. This is perhaps particularly pertinent for CRC survivors, for whom evidence is strong that their cancer is related to diet- and exercise-related lifestyle choices.54,55 As the population of survivors grows, issues concerning their long-term care, including managing health behavior risks, will become increasingly important.
The authors indicated no potential conflicts of interest.
Conception and design: Susan A. Sabatino, Ralph J. Coates, Robert J. Uhler, Lori A. Pollack, Linda G. Alley, Laura J. Zauderer Financial support: Ralph J. Coates Administrative support: Susan A. Sabatino, Ralph J. Coates Collection and assembly of data: Ralph J. Coates, Robert J. Uhler Data analysis and interpretation: Susan A. Sabatino, Ralph J. Coates, Robert J. Uhler, Lori A. Pollack, Linda G. Alley, Laura J. Zauderer Manuscript writing: Susan A. Sabatino, Ralph J. Coates, Lori A. Pollack, Linda G. Alley, Laura J. Zauderer Final approval of manuscript: Susan A. Sabatino, Ralph J. Coates, Robert J. Uhler, Lori A. Pollack, Linda G. Alley, Laura J. Zauderer
We thank Trevor Thompson for his assistance in revising this manuscript.
Supported by an appointment to the Research Participation Program at the Centers for Disease Control and Prevention (CDC) administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the US Department of Energy and CDC (S.S.). Presented in part at the 2006 International Union Against Cancer (UICC) World Cancer Congress, July 11, 2006, Washington, DC. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the funding agency. Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.
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Copyright © 2007 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
25.0), physical activity (recommended levels defined as 
