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Published OnlineFirst January 16, 2013; DOI: 10.1158/1940-6207.CAPR-12-0385

Cancer Prevention Review Research

Promoting Changes in Diet and Physical Activity in and Colorectal Settings: An Unexplored Opportunity for Endorsing Healthy Behaviors

Annie S. Anderson, Dionne Mackison, Callum Boath, and Robert Steele

Abstract The importance of diet, physical activity, and weight management in breast and colorectal cancer prevention is widely recognized. While there may be many "teachable moments" that could be used to assess and initiate changes in these behaviors by health professionals (to complement public health campaigns), there is little evidence that lifestyle is discussed within settings. The lack of advocacy about lifestyle in these settings may endorse poor health behaviors, in particular the absence of guidance to visibly obese patients. To fully use the teachable moment, patients need to be aware of the relationship between diet and physical activity and the risk of cancer and to be able to relate guidance to personal behaviors. Results from cardiovascular and diabetes prevention programs provide evidence about the components of effective behavior change programs which could be used in the screening setting. Findings from interventions initiated in the colorectal cancer screening setting suggest that such programs can be delivered but it is not clear how acceptable these are in routine health services. Effective interventions delivered in this setting also offer an important opportunity to contribute to the reduction of the overall burden of chronic non-communicable diseases. Cancer Prev Res; 6(3); 165–72. 2013 AACR.

Introduction The general public perceive health professionals as The role of food, nutrition, physical activity, and the experts in matters relating to disease prevention and man- prevention of cancer has been extensively reviewed (1), agement; thus individual patient communications on and estimates for disease reduction indicate that around health behaviors can endorse the messages of public health one third (2) of the most common could be campaigns. Advocacy for changing health behaviors by prevented by changes in these health behaviors (in addi- health professional organizations and individual profes- tion to reductions achieved through tobacco control). sional action (including acting as role models) has been There have been many efforts to change diet and physical widely used in tobacco control and has been considered an activity behaviors through public health education pro- important contributor to gaining support for the develop- grams, but it is clear that moving evidence on lifestyle and ment of meaningful government policies. Although there is cancer prevention to everyday practice and policy needs widespread recognition that health promotion is central to the synergy of actions from a wide range of stakeholders. the provision of health care (4), the potential of health care For example, The American Cancer Society (3) make systems (including hospitals and clinics) to promote appro- community action recommendations to create a support- priate diet, physical activity, and body weight is an area that ive social and physical environment to facilitate healthful is largely underdeveloped. Recent initiatives such as the behavior change. In addition, the World "health promoting health service" and "every contact Fund/American Institute for Cancer Research (2) high- counts" in the United Kingdom provide opportunities to lights 9 stakeholder communities (e.g., health profes- deliver evidence-based programs. sionals, media, government, schools) for concerted action. Cancer screening and early detection services as an opportunity for endorsing lifestyle change by health professionals Authors' Affiliation: Centre for Research into Cancer Prevention and In 2008, Demark-Wahnefried and colleagues (5) pub- Screening, Ninewells Medical School, University of Dundee, Scotland, United Kingdom lished guidance for physicians on advising patients about cancer prevention and lifestyle including taking advantage Corresponding Author: Annie S. Anderson, University of Dundee, Mailbox 7, Ninewells Hospital, Dundee, Scotland DD1 9SY, United Kingdom. of teachable moments (e.g., before and after cancer screen- Phone: 441382383299; Fax: 441382632333; E-mail: ing, on the diagnosis of a premalignant lesion and after the [email protected] diagnosis of cancer in patients or their family members), but doi: 10.1158/1940-6207.CAPR-12-0385 there is little evidence that such interventions take place on a 2013 American Association for Cancer Research. routine basis. It is timely therefore to review factors that may

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Anderson et al.

impact on diet and physical activity interventions for cancer (i.e., suspicious for cancer) results for screen-detected risk reduction within early detection (screening) settings polyps tended to reduce their smoking habits and had a and consider ways to maximize the potential for promotion smaller increase in body mass index (BMI) over a 13-year of behavior change in these arenas. period than those with negative (i.e., normal) results. In A number of studies have assessed lifestyle behaviors in their review of screening and lifestyle behaviors, Van der patients attending cancer screening/early detection services Aalst and colleagues (15) concluded that the psychologic although these largely relate to lung and cervical cancer impact of screening peaks shortly after screening but then screening and smoking. In breast and colorectal cancer, diet, returns to baseline values in the long-term and careful alcohol, physical activity, and excess body weight have been consideration should be given to timing of health promo- implicated in etiology. Therefore, discussion of these beha- tion interventions. viors can relate directly to site-specific cancer risk reduction Referrals to early detection services may also arise through and provide some justification for lifestyle communications family history and procedures. A family within these respective screening programs. may be a powerful motivator to consider It is recognized that lifestyle interventions in the screen- disease risk and a stimulus to engage in healthy lifestyles ing setting will only reach people who choose to participate (including screening). However, it is unlikely that family in such programs. In many cases, this means people from history per se is sufficient to avoid high-risk behaviors. areas of low social deprivation with higher education levels Spector and colleagues (16) reported that in 50,844 black and better access to affordable health care. It might be and white women who had a sister with , there hypothesized that participants are more likely to have were no indications that they were more likely to engage in favorable health behaviors. However, a number of studies healthy lifestyle behaviors than the general population. (6, 7) in the colorectal screening domain have reported Likewise, in a study of health and lifestyle behaviors among inappropriate dietary intakes, levels of physical activity, and persons at risk of Lynch syndrome, Burton and colleagues body weight among screening participants. In addition, (17) reported that 10% of 319 people with the disease and disease screening has been said to awaken curiosity about 20% of 110 unaffected relatives reported 3 or more risk health conditions and provides an opportunity to consider behaviors with 20% and 12%, respectively, reporting zero preventative actions (8). risk behaviors. Higher risk behavior scores were associated In the breast cancer setting, advice on diet and exercise is with being male, having less education, and age less than 50 not routinely provided although there is evidence that years. While there are no trials to show that lifestyle change women would welcome this (9). This issue may be partic- would specifically reduce colorectal cancer risk in this ularly relevant for body weight, where the lack of guidance patient subgroup, such changes are likely to provide overall to visibly obese patients may signal lack of medical concern. health benefits. The authors concluded that genetic counsel- It is recognized that there are challenges in discussing weight ing offers a promising avenue for education and behavioral management in a clinical setting and that staff may be risk reduction in persons with familial or genetic predispo- uneasy about confronting patients with the issue of weight sition. Current work in the genetic screening arena is management, especially if their training has not included focused on encouraging patients to undertake cancer guidance on how to broach the topic or how to apply screening procedures and there is little evidence of promo- intervention techniques. There is, however, some evidence tion of healthy lifestyles, but this setting offers the oppor- that people may find it more acceptable to discuss the topic tunity to discuss the importance of healthy lifestyle at a time with health care staff rather than with friends or peers (10) when patients are focused on the disease rather than in the and may respond positively to intervention advice from general context of having a family history of cancer. health care professionals. Research from the colorectal cancer screening environ- Delivering lifestyle programs in screening settings— ment (11, 12) indicates that patients diagnosed with ade- can it be done? nomas are not exposed to prevention messages within the The largest program of lifestyle interventions delivered in clinical colonoscopy setting. The lack of advocacy on life- collaboration with early cancer detection services is the style change in these settings may in fact endorse poor American "Well-Integrated Screening and Evaluation for health behaviors as it is recognized that the absence of Women Across the Nation" (WISEWOMAN) program guidance may produce a "health certificate effect" so that which targets low-income, under- and uninsured women patients who receive negative (i.e., no abnormally detected) ages 40 to 64 years. The program works in conjunction with results may feel no need to modify their lifestyle (13). the National Breast and Cervical Cancer Early Detection Larsen and colleagues (13) reported observational findings Program (NBCCEDP) and aims to reduce cardiovascular for a range of lifestyle behaviors in colorectal cancer screen- risk by providing screening for high blood pressure, hyper- ing which indicated that a negative (i.e., normal) screening cholesterolemia, and abnormal glucose levels and deliver outcome was significantly associated with weight gain and lifestyle interventions on diet, physical activity, and smok- control subjects (people who has not undergone screening) ing. is also provided, although the had significantly better improvements in smoking habits relationship between results and lifestyle risk are not known and exercise after a 3-year follow-up period. However, to be discussed. Early research results indicated that the Hoff and colleagues (14) found that patients with positive program had been successful in reducing hypertension,

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Promoting Lifestyle Change in Screening Settings

BMI, and dietary fat as well as increasing physical activity in relating to a range of dietary components and body size. this hard to reach group. Between 2008 and 2010, it is Ongoing work in this arena (24) includes a focus on weight estimated that 43,000 women participated in at least one management with guidance on dietary composition and lifestyle intervention session (18). This program shows physical activity to achieve weight targets in patients diag- the feasibility of bringing early detection services and life- nosed with colorectal . style activities together to support changes in health beha- Most interventions have used health behavioral theories viors. However, the focus on cardiovascular risk may miss (ref. 25; e.g., The Theory of Planned Behaviour, Trans- the opportunity to fully develop concepts of cancer preven- theoretical model, Social Learning Theory) to guide educa- tion. For example, current evidence suggests that modest tional, motivational, and behavioral strategies. The delivery alcohol intakes >10 g/d are associated with increased breast of the interventions have varied in intensity and commu- cancer risk (1) but may confer cardioprotective effects and nication media and have shown less reliance on traditional, lead to confusion on risk versus benefits of alcohol face to face counseling with a greater emphasis on mailed consumption. and telephone delivery routes. All approaches have used Despite the association between physical inactivity, alco- some form of personal assessment of the target behavior hol, and obesity in the etiology of breast cancer, few studies and tailored (personalized) feedback. have reported using the breast cancer screening/early detec- All the intervention studies have reported significant tion setting to promote diet and exercise interventions for effects on the target behaviors, although these have been primary prevention of cancer. Friedenrich and colleagues modest with the exception of Smith-Warner and colleagues (19) recruited women in the ALPHA study of exercise (23) who reported an increase from 7.3 servings of fruits intervention on adiposity outcomes through targeted mail- and vegetables at baseline to 11.9 servings at 12 months of ings to the Alberta Breast Screening Programme but also follow-up. However, it is notable that the baseline intake used posters and brochures distributed to family physicians was not far off the goal of 8 servings/d (7.3 and 6.7 servings and media campaigns. In total, 320 postmenopausal in the intervention and control groups, respectively) which women ages 50 to 74 years were randomized to undertake suggest that participants were already showing considerable 45 minutes of moderate to vigorous exercise 5 times a week. care in dietary choices. Overall, these studies suggest that The intervention included 3 facility-based sessions and a diet and physical activity interventions in these settings are comprehensive educational package, incentives, regular successful in promoting changes in these behaviors. How- newsletters, and a website. Women in the control group ever, it is likely that more intensive approaches may be were asked to maintain their regular activity and all parti- needed to address weight management issues. cipants were asked not to change their diet. After a 1-year In addition, it is not clear how applicable or acceptable follow-up period, the intervention groups showed signifi- these approaches might be in routine early cancer detection cantly greater losses in adiposity markers (body weight, settings for the general population. For example, the pro- body fat, subcutaneous abdominal fat) than in control portion of people approached about the intervention stud- participants. It is notable that of 3,454 women assessed for ies who were then randomized varied from 22% (23) to eligibility, 320 were randomized (1,840 failed to meet the 67% (22). Smith-Warner and colleagues (23) reported eligibility criteria) so while this study completed its aims in reasons for not wishing to take part as "lack of interest" terms of efficacy, it may not be fully predictive of population (38%), "time and travel constraints" (14%), and medical effectiveness. reasons (9%). It is plausible that some of these responses A number of intervention studies (7, 20–23) focusing on reflect lack of interest in the study procedures (e.g., mea- diet and physical activity behaviors in cancer prevention surement procedures) although the findings suggest that have been delivered in conjunction with colorectal cancer intervention programs need to take account of barriers to early detection investigations or screening programs (Table engagement and to identify routes to increase interest in the 1). Most studies have targeted older adults when the disease target population is more likely to present and most studies have succeeded in recruiting men (who are generally considered to be less Lessons from diabetes and cardiovascular disease interested in preventative behaviors). Some, but not all, One reason for lack of diet and physical activity programs interventions have been offered to people with adenomas, in cancer care settings may be related to skepticism from so that perceived cancer risk is likely to have varied between health care professionals about the ability of individuals to study groups. In addition, some studies have recruited change their diet and physical activity levels. However, asymptomatic screening patients who are more likely to results from diabetes prevention programs (26) have shown engage in prevention behaviors, whereas others studies that, with appropriate support, these behaviors can be have recruited patients referred for colonoscopy due to altered with significant clinical effects. Likewise, in the symptoms who may be motivated to have medical treat- cardiovascular arena, it has been shown that individual ments but have less interest in preventative behaviors. dietary interventions in primary prevention can achieve It is notable that the most common dietary focus has been modest improvements in diet and cardiovascular disease on increasing intakes of fruits and vegetables. Most of these risk status (27). Although both diabetes and cardiovascular studies were conducted before the WCRF report of 2007 (1) prevention research have the advantage of early disease and have not fully taken account of more recent evidence biomarkers and the capability to show the impact of

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Intervention delivery procedures/ First author Number of Characteristics Early detection Behavioral behavioral strategies/ Follow-up

cancerpreventionresearch.aacrjournals.org (reference) Country subjects of participants setting focus behavioral theory period Results Published OnlineFirstJanuary16,2013;DOI:10.1158/1940-6207.CAPR-12-0385 Baker and 742 55–64 y Flexible Fruits and Mailed 6 wks Intervention (IV) vs. control colleagues (20) sigmoidoscopy vegetables UK ( status unknown) 373 female Brief 2 page tailored, Daily fruit servings increased psycho-educational significantly more in IV group intervention (þ0.59; CI, 0.47–0.71) vs. (þ0.14; CI, 0.03–0.026) 355 male Stages of change Daily vegetable servings increased significantly more in IV group (þ0.47; CI, 0.36–0.59) vs. Cancer Research. (þ0.12; CI, 0.01–0.23) Total daily servings increased significantly more in IV group (1.06; CI, 0.87–1.25) vs. (0.26; CI, on September 28, 2021. © 2013American Association for 0.08 to 0.25) Caswell and 74 50–69 y Colorectal cancer Physical activity One personal contact 3 mo Intervention vs. control: colleagues (21) screening (with plus mailed literature UK adenomas) 22 female Fruits and Tailored goals, social Fiber intake score significantly vegetables support identified increased from (30 11 to 41 feedback. 113) vs. no change in control (31 8to30 11) where score <30 equals <20 g/d, 30–40 equals 21–30 g/d, >40 equals >30 g/d) 52 male Cereal fiber Focus on self-efficacy Fruit and vegetable intake

acrPeeto Research Prevention Cancer increased from 4.8 2.5 to 7.9 3.1 portions/d vs. 4.8 3.1 to 7.3 4.2 (NS). Physical activity increased from 50 49 to 85 72 vs. 68 74 to 79 70 mins/d (NS) IV achieving all 3 lifestyle recommendations increased significantly to 47% vs. 13% (Continued on the following page) www.aacrjournals.org Downloaded from Table 1. Diet and physical activity interventions in colorectal cancer early detection/screening settings (Cont'd )

Intervention delivery procedures/ First author Number of Characteristics Early detection Behavioral behavioral strategies/ Follow-up (reference) Country subjects of participants setting focus behavioral theory period Results cancerpreventionresearch.aacrjournals.org Emmons and 1247 40þ y Colonoscopy/ Red meat Initial telephone delivery 8 mo Intervention vs. control Published OnlineFirstJanuary16,2013;DOI:10.1158/1940-6207.CAPR-12-0385 colleagues (7) flexible (motivational and goal USA sigmoidoscopy setting), plus4 (with adenomas) monthly telephone counseling calls. Computer-generated tailored print progress reports, tailored self- help materials 523 female Fruits and Social cognitive theory Multiple risk factor score vegetables significantly reduced by 47% vs.

Cancer Research. 35% 724 male Multivitamin Significant differences in red intake meat (reduction) and (increased) multivitamin usage and physical activity risk factors on September 28, 2021. © 2013American Association for Alcohol use No significant differences in smoking, alcohol, fruits and vegetable risk factors Physical activity

Robb and 365 58–59 y Flexible Fruits and Mailed standard leaflet 6 mo Intervention vs. control Settings Screening in Change Lifestyle Promoting colleagues (22) sigmoidoscopy vegetables intervention UK (no adenomas) 215 female Physical activity or Five a day intake increased significantly more in tailored

acrPe e;63 ac 2013 March 6(3) Res; Prev Cancer group (9% vs. 2% in standard care and 5% decrease in control). OR, 2.28; CI, 1.09–4.96 150 male Alcohol Mailed standard leaflet Those meeting recommended plus tailored physical activity increased by feedback with praise/ 7% in the tailored group vs. 2% encouragement standard care and 1% control NS No change in alcohol (Continued on the following page) 169 Published OnlineFirst January 16, 2013; DOI: 10.1158/1940-6207.CAPR-12-0385

Anderson et al.

interventions in relatively short-term periods, the method- ologies for supporting behavior change remain relevant for 2.8 to

cancer prevention and control.

3.3 to 11.9 The necessary components for lifestyle modification (including weight management) in diabetes prevention cant)

fi trials have been reported as provision of 4 to 6 months of frequent intervention contact to achieve at least 5% body weight reduction with feedback and social support deliv- 2.2 ered for sustained weight loss (28). Out-with the intensive

3.3 portions/d vs. 6.7 trial setting, the nationwide Finnish Type 2 Diabetes Pre- vs. 17% (signi 6.2 increased from 7.3 vention program (FIND2D) uses a brief (14 question) risk Fruit and vegetable intake Target intake was met by 86% assessment tool, behavioral strategies, individual counsel- ing or group visits and has already shown significant weight loss and reduction of diabetes. While this type of interven- tion could not easily be delivered within all early cancer Follow-up period Results 12 mo Intervention vs. control detection settings, there may still be the opportunity to deliver brief interventions (as a form of endorsement for behavior change) with referral to relevant community- based intervention programs. Whilst there is significant evidence available on poten- tially effective approaches for effective lifestyle change, this area deserves further exploration as new technologies (e.g., web-based programs, smart phones) and social media com-

(nutrition counseling) monitoring, feedback, memory prompts, social support munications are developed. Intervention delivery procedures/ behavioral strategies/ behavioral theory Face to face meeting Goal setting, self- Social learning theory

Moving forward: challenges to address in promoting changes in diet and physical activity in early cancer detection settings It is plausible that behavior change programs which target

vegetables (8 servings/d) high-risk groups are more effective than those targeting the Behavioral focus Fruits and population at large. Thus, adults who have had a "health scare" may experience a "teachable moment" and will be more motivated to engage in and adhere to lifestyle advice. However, Stead and colleagues (11) have argued that after diagnosis of a colorectal adenoma. patients need to be aware of the risk factors for adenoma and relate these to personal behaviors before the teachable moment opportu- adenomas) nity can be used. They also noted that while there is a shared Early detection setting Colonoscopy (with and accepted understanding of the relationship between smoking and lung cancer, there is much less awareness of the relationship between colorectal cancer, diet, and phys- ical activity. The lack of communications on lifestyle messages by colorectal cancer professionals and missed 74 y – opportunities for advocacy were also reported by Stead and Characteristics of participants 30 145 male 57 female colleagues (11). These findings have been echoed by Dowswell and col- leagues (12) who found that patients ages 60 to 74 years who had been diagnosed with an intermediate- or high-risk adenoma believed that their current dietary and physical 202 Number of subjects activity behaviors were good and they perceived no risk between current health behavior and diagnosis. They sug- gested that intervention programs should tailor the inter- vention to individuals and target the lack of knowledge Diet and physical activity interventions in colorectal cancer early detection/screening settings (Cont'd ) about the etiology of colon cancer and the lack of motiva- tion to change behavior. One useful development in this area could be routine use of lifestyle risk assessment (29) colleagues (23) USA and feedback (already used in diabetes prevention) deliv- Smith-Warner and Table 1. First author (reference) Country ered as part of cancer screening which has the potential to

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Promoting Lifestyle Change in Screening Settings

increase engagement with health promotion. control strategy which presents a unique opportunity physical activity intervention programs in early detection for endorsement of consistent lifestyle messages from settings based on health behavior theory have been reported respected cancer health care professionals. This approach to improve diet more effectively than those without a also offers an important opportunity to contribute to the theoretical basis (30). While the optimal intensity and reduction of the overall burden of chronic noncommunic- format of intervention communications is unclear, mini- able diseases. mal contact procedures have been shown to initiate health behavior change and offer the opportunity for widespread Disclosure of Potential Conflicts of Interest engagement. In addition, many existing community-based No potential conflicts of interest were disclosed. interventions (e.g., walking groups) offer opportunities for engaging in lifestyle change. Authors' Contributions However, intervention programs are often less likely to Conception and design: A.S. Anderson, R. Steele reach the most vulnerable population groups (including Development of methodology: A.S. Anderson, D. Mackison men) who are also less likely to participate in early detection Acquisition of data (provided animals, acquired and managed patients, provided facilities, etc.): A.S. Anderson, R. Steele services. Although this review has focused on diet and Analysis and interpretation of data (e.g., statistical analysis, biosta- physical activity, it is possible that targeting multiple risk tistics, computational analysis): A.S. Anderson, C. Boath factors may maximize the impact of the intervention (31), Writing, review, and/or revision of the manuscript: A.S. Anderson, D. Mackison, C. Boath, R. Steele but there is little evidence to support this approach as a Administrative, technical, or material support (i.e., reporting or orga- population-wide strategy given the difficulties that many nizing data, constructing databases): D. Mackison, C. Boath people have in achieving even one lifestyle change goal. Study supervision: A.S. Anderson, R. Steele Building bridges between cancer prevention and screen- Received September 11, 2012; revised December 22, 2012; accepted ing should be seen as one strand of a multicomponent December 28, 2012; published OnlineFirst January 6, 2013.

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Promoting Changes in Diet and Physical Activity in Breast and Colorectal Cancer Screening Settings: An Unexplored Opportunity for Endorsing Healthy Behaviors

Annie S. Anderson, Dionne Mackison, Callum Boath, et al.

Cancer Prev Res 2013;6:165-172. Published OnlineFirst January 16, 2013.

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