Proposal:Breast Cancer in Hispanic Populations

Survivorship care plans and adherence to lifestyle recommendations among breast cancer survivors

Heather Greenlee1,2 & Christine L. Sardo Molmenti1,2 & Katherine D. Crew1,2,3 & Danielle Awad2 & Kevin Kalinsky2,3 & Lois Brafman2 & Deborah Fuentes2 & Zaixing Shi1 & Wei-Yann Tsai2,4 & Alfred I. Neugut1,2,3 & Dawn L. Hershman1,2,3

Received: 19 February 2016 /Accepted: 31 March 2016 /Published online: 21 April 2016 # Springer Science+Business Media New York 2016

Abstract Purpose The effectiveness of survivorship care plans has not been widely tested. We evaluated whether a one-time brief lifestyle consultation as part of a broader survivorship care plan was effective at changing diet and lifestyle patterns. Methods A diverse sample of women with stage 0-III breast cancer were randomized to control or intervention groups within 6 weeks of completing adjuvant treatment. Both groups received the National Cancer Institute publication, BFacing Forward: Life after Cancer Treatment.^ The intervention group also met with a nurse (1 h) and a nutritionist (1 h) to receive personalized lifestyle recommendations based upon national guidelines. Diet, lifestyle, and perceived health were assessed at baseline, 3 and 6 months. Linear regression anal- yses evaluated the effects of the intervention adjusted for covariates. Results A total of 126 women completed the study (60 control/66 intervention, 61 Hispanic/65 non-Hispanic). At 3 months, the intervention group reported greater knowledge

of a healthy diet (P=0.047), importance of physical activity (P = 0.03), and appropriate use of dietary supplements (P=0.006) and reported lower frequency of alcohol drinking (P=0.03) than controls. At 6 months, only greater knowledge of a healthy diet (P=0.01) persisted. The intervention was more effective among non-Hispanics than Hispanics on im- proving attitude towards healthy eating (P =0.03) and fre- quency of physical activity (P=0.006). Conclusions The intervention changed lifestyle behaviors and knowledge in the short-term, but the benefits did not persist. Implications for Cancer Survivors Culturally competent long-term behavioral interventions should be tested beyond the survivorship care plan to facilitate long-term behavior change among breast cancer survivors.

Keywords Survivorship care plan . Breast cancer . Diet .

Physical activity . Dietary supplements

Introduction

Of the estimated 14.5 million cancer survivors in the USA in 2014, more than three million are breast cancer survivors [1], a number that continues to increase [2]. The 5-year survival rate of breast cancer is approximately 89 % [3], and breast cancer currently represents the largest group of survivors (22 %) [1]. Compared to non-Hispanic white women, Hispanic breast cancer survivors have higher rates of breast cancer recurrence and poorer survival, even when estimates are adjusted for age and stage at diagnosis [4].

There is a compelling link between post-diagnosis lifestyle habits and breast cancer outcomes. A growing body of evi- dence suggests that a healthy diet, regular physical activity, and a normal body weight are associated with better breast cancer outcomes. However, there are few effective clinical

Prior presentation Poster presentation at San Antonio Breast Cancer Symposium, December 2013

* Heather Greenlee [email protected]

1 Department of Epidemiology, Mailman School of Public Health, Columbia University, 722 W. 168th Street, New York, NY 10032, USA

2 Herbert Irving Comprehensive Cancer Center, Columbia University, New York, NY, USA

3 Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, NY, USA

4 Department of Biostatistics, Mailman School of Public Health, Columbia University, New York, NY, USA

J Cancer Surviv (2016) 10:956–963 DOI 10.1007/s11764-016-0541-8

models for helping women achieve and maintain the diet, physical activity, and body weight guidelines set forth by na- tional organizations, including the American Cancer Society and the American Institute for Cancer Research [5, 6].

According to the 2006 Institute of Medicine (IOM) report entitled, BFrom Cancer Patient to Cancer Survivor: Lost in Transition,^ all patients completing primary treatment for can- cer should receive a survivorship care plan, and the Commission on Cancer now requires survivorship care plan implementation [2, 7]. According to these guidelines, survi- vorship care plans should focus on five content areas, one of which emphasizes preventive practices and recommendations for healthy living after cancer treatment based upon the American Institute for Cancer Research guidelines [2]. Breast cancer survivors are key populations to target for sur- vivorship care plans due to the high prevalence and incidence of this disease [8] and the potential for affecting a large num- ber of cancer survivors.

Survivorship care plans have been widely implemented by multiple organizations in the USA and abroad [9–14], yet data evaluating the efficacy of this intervention on patient out- comes are limited and have shown inconsistent results [8, 15]. Our group previously reported on a single-blinded ran- domized controlled trial with the a priori objective of exam- ining the effect of an in-person survivorship care plan inter- vention following adjuvant breast cancer therapy on health worry, treatment satisfaction, and the impact of cancer [16]. However, few studies have evaluated the efficacy of survivor- ship care plans on post-treatment diet and lifestyle behavior change.

We compared the effects of a single 2-h survivorship counseling session (1 h with nurse and 1 h with nutritionist) vs. printed materials on diet and lifestyle knowledge and behaviors.

Patients and methods

Participants

All participants were recruited from the Columbia University Medical Center (CUMC) breast oncology clinic. Eligible par- ticipants were English- and Spanish-speaking women with a history of stage 0–III breast cancer and who were within 6 weeks of completion of initial adjuvant treatment (radiation or chemotherapy). Patients were ineligible if they received surgery alone without adjuvant therapy or had a significant psychiatric illness that precluded the completion of the study questionnaire. Hispanic women were oversampled to achieve an approximate equal number of Hispanic and non-Hispanic participants. All participants provided written informed con- sent in English or Spanish. The clinical trial was approved by

the local Institutional Review Board (ClinicalTrials.gov num- ber: NCT00821288).

Data collection

At baseline, participants completed brief questionnaires on attitudes, knowledge, and behaviors related to diet, physical activity, and use of dietary supplements. The questions were designed to be brief assessments of each construct and were created specifically for this study. At 3 and 6 months, both groups completed in-person questionnaires on diet and life- style attitudes, knowledge, and behaviors.

Randomization

This single-blinded randomization study has been described previously [16]. In brief, women were randomized to a survi- vorship intervention group or control group. Randomization was stratified by Hispanic ethnicity, and a block randomiza- tion list was created using a computer-generated sequence for each of the stratification groups. Because the study posed minimal risk and to control for knowledge of intervention assignment, participants were told that they were participating in a cancer survivorship study and were blinded to randomi- zation assignment.

Intervention

The research staff provided all subjects in control and inter- vention arms with the National Cancer Institute (NCI) publi- cation, BFacing Forward: Life after Cancer Treatment^ [17]. This 24-page printed guide (available in Spanish and English) summarizes several key issues of interest to cancer survivors, such as receiving follow-up medical care and strategies for managing physical changes, potential symptoms, healthy life- style habits, feelings, and social and work relationships.

In addition to receiving this guide, the survivorship inter- vention group met with a nurse (1 h) to receive a treatment summary and surveillance recommendations based on the American Society of Clinical Oncology guidelines and a nu- tritionist (1 h) to receive personalized lifestyle recommenda- tions based on nutrition and physical activity guidelines de- veloped by the American Institute for Cancer Research and the American Cancer Society [5, 6]. All study materials were provided in Spanish and English, depending on participant preference. Nursing staff were bilingual, and the nutritionist used an interpreter.

Statistical analysis

Demographic, clinical, and outcome variables were described using means and standard deviations for continuous variables and percentages for categorical variables, by treatment group

J Cancer Surviv (2016) 10:956–963 957

and by ethnicity. Linear regression analyses adjusted for eth- nicity evaluated the effects of the intervention on knowledge and uptake of diet and lifestyle recommendations (model 1). Additional models evaluated the interaction between interven- tion and ethnicity (model 2).

Results

A total of 317 women were screened, 141 were randomized, and 126 women completed the study (60 control; 66 interven- tion), as has been previously reported [16]. Baseline demo- graphic and clinical data are presented in Table 1. The mean age of participants was 54 years and 48 % self-identified as Hispanic. There was no imbalance in demographic and clini- cal characteristics between intervention arms. Compared to non-Hispanics, Hispanics were less likely to attend college, less likely to be married, less likely to have full-time employ- ment, and reported lower income. In addition, Hispanics re- ported poorer knowledge of healthy lifestyle behaviors (e.g., diet, physical activity, weight, dietary supplements), lower intake of fruits and vegetables, less recreational physical ac- tivity, lower consumption of alcohol, and a lower overall health rating (all P<0.05, data not shown).

Attitudes towards lifestyle behaviors

The intervention was not associated with changes in any atti- tudes towards lifestyle behaviors related to general health (Table 2). In models assessing an interaction between inter- vention condition and ethnicity, compared to Hispanics, the intervention had a stronger effect on increasing non- Hispanics’ belief that a healthy diet was important to prevent breast cancer recurrence (Table 2) (mean change in a scale of 1–5 with higher score indicating greater knowledge: non- Hispanic: 0.31 vs. Hispanic: −0.31, P=0.03). No effects were observed at 6 months.

Knowledge of lifestyle behaviors

In analyses adjusted for ethnicity, at month 3, the intervention group compared to the control group reported greater knowl- edge of how to eat a healthy diet (mean score on a scale of 1–5 with higher score indicating greater knowledge: intervention: 4.2 vs. control: 4.0, P=0.047), greater knowledge of getting enough physical activity (mean score: intervention: 3.2 vs. control: 2.7, P=0.03), and greater knowledge of appropriate use of dietary supplements (mean score: intervention: 3.8 vs. control: 3.3, P=0.006) (Table 2 and Fig. 1). At month 6, the only difference that persisted was greater knowledge of a healthy diet (mean score: intervention: 4.3 vs. control: 4.0, P=0.01).

Frequency of lifestyle behaviors

In analyses adjusted for ethnicity, at month 3, the intervention group reported lower frequency of alcohol drinking (mean weekly frequencies: intervention: 0.9 vs. control: 1.6, P=0.03) (Table 2 and Fig. 1). Compared to Hispanics, the intervention had a stronger effect on increasing frequency of physical activity in non-Hispanics (mean change in weekly frequencies: non-Hispanic: 1.21 vs. Hispanic: −0.87, P=0.006). No effects were observed at 6 months.

Discussion

Survivorship care plans are required by the Commission on Cancer Standard 3.3 [7], despite limited evidence on efficacy or an understanding of the best method to the plans. Survivorship care plans are not standardized across institu- tions, and the effectiveness of various components of plans has not been evaluated in many studies. Simultaneously, the importance of healthy lifestyles following cancer diagnosis and during survivorship is of growing interest to cancer pa- tients, and the effectiveness of lifestyle interventions in the oncology clinical setting has not been widely evaluated. Within a randomized controlled trial testing the effectiveness of a survivorship care plan on the quality of life and patient satisfaction in a diverse population of breast cancer survivors, we tested the effectiveness of a brief behavioral intervention (1 h with nurse and 1 h with nutritionist) on changing knowl- edge and behaviors related to diet, physical activity, and use of dietary supplements. We found that the intervention changed lifestyle behaviors and knowledge in the short-term, but the benefits did not persist. In addition, we found that the inter- vention was more effective in non-Hispanic whites than in Hispanics. We conclude that longer and more intensive behav- ioral interventions may be needed to achieve and sustain be- havior change.

The majority of survivorship care plan studies have not been randomized, and behavior change studies related to can- cer survivorship care plans are limited; however, the evidence base is growing. In a recent cluster randomized controlled trial, Nicolaije et al. reported that cancer survivors who re- ceived an automatically generated survivorship care plan re- ported more cancer treatment knowledge, awareness of cancer-related symptoms, and communication with primary care physicians, suggesting that a cancer survivorship care plan may increase adherence to recommended breast cancer survivorship care [15]. In the Wellness Beyond Cancer Program (WBCP) [18], qualitative surveys were mailed to all patients and primary care providers (PCPs) 1 year after patients were referred to the program to evaluate patient and primary care provider satisfaction with the survivorship pro- gram. The median satisfaction scores were consistently high

958 J Cancer Surviv (2016) 10:956–963

1 year post-discharge, indicating that the PCPs and patients were highly satisfied with the program content. The authors

mentioned potential areas for improvement in the areas of communication and dissemination of cancer-related

Table 1 Baseline demographic and clinical characteristics Intervention arm Ethnicity

Intervention Control P value*

Hispanic Non- Hispanic

P value*

(n = 66) (n = 60) (n = 61) (n = 65)

Demographic characteristics

Age, years, mean (SD) 53.7 (12.1) 54.9 (10.9)

0.55 53.2 (11.3)

55.1 (11.8) 0.35

Race, % 0.38 <0.0001

White 59 58 32 83

Black 23 30 51 5

Asian 2 5 0 6

American Indian 2 0 0 2

Other 14 7 17 5

Hispanic ethnicity, % 52 45 0.46 100 0 –

Education, % 0.89 <0.0001

Grade school 15 19 33 2

High school 26 25 35 17

College 38 32 27 43

Graduate school 21 24 5 38

Marital status, % 0.37 <0.001

Single 26 20 29 17

Married/partnered 57 53 41 69

Divorced/separated 11 22 20 12

Widowed 6 5 10 2

Employment, % 0.87 <0.01

Full-time 33 35 22 46

Part-time/self-employed 14 19 12 20

Unemployed 14 12 20 6

Other 39 34 46 28

Income, % 0.78 <0.0001

0–$30,000 39 42 70 18

$30,001–60,000 16 10 15 11

$60,000–100,000 19 23 9 31

<$100,000 26 25 6 40

Clinical characteristics

Post-menopausal, % 74 73 0.98 67 80 0.11

Stage, % 0.17 0.07

0 3 1 5 0

I 46 50 39 55

II 38 36 39 37

III 13 13 16 8

Chemotherapy, % 77 71 0.41 74 78 0.54

Radiation therapy, % 70 73 0.75 77 70 0.24

Hormonal therapy, % 83 74 0.20 70 85 0.06

Abbreviations: SD standard deviation

*P values calculated using t tests (continuous measures), Fisher’s exact tests (categorical measures with expected cell counts <5), and chi-squared tests (categorical measures)

J Cancer Surviv (2016) 10:956–963 959

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960 J Cancer Surviv (2016) 10:956–963

information to PCPs. A recent systematic review focused on survivorship care plan preferences of cancer survivors and health care providers but did not address lifestyle factors or evaluate behavior change [19]. The review included 19 quan- titative studies (14 questionnaires, 1 pilot study, 1 online tool, and 3 randomized clinical trials) and 10 qualitative studies (focus groups and interviews). Sample sizes of the studies ranged from 34 to 2250 survivors. The conclusions of the systematic review did not illuminate any consistent preferences or specific items that would be useful to include on treatment summaries or survivorship care plans according to providers and survivors. This may be in large part due to the less than robust studies available/included in this review.

Other studies have evaluated the success of survivor- ship care plan implementation in various settings, includ- ing the oncology team, the primary care provider, and within a comprehensive cancer center. A recent report de- scribes specific, implemented cancer survivorship activi- ties developed and incorporated by grantees of CDC’s National Comprehensive Cancer Control Program (NCCCP) [20]. The report indicates that among four state-level and one tribal grantees, there are numerous

activities underway aimed at improving communication between the oncology team and the primary care provider, enhancing education and training, and implementing new programs, policies, and infrastructure. This report further highlights activities within Comprehensive Cancer Control programs that offer survivorship care plans and support an important role for the primary care provider in this setting, as noted in a previous study by Westfall et al. [20, 21]. While the drawbacks of this model, including the time and the lack of a standardized model for implementation are notwithstanding, more recent data shows a general in- terest among integrated health systems to incorporate sur- vivorship care plans [22]. Novel methods for the rapid creation and delivery of survivorship care plans within an integrated health system utilizing electronic medical record are being explored [23]. Lessons learned while finding seamless and efficient ways to integrate and implement survivorship care plans have been reported in other studies [24]. Many of these barriers may be overcome by organiz- ing a multi-disciplinary team to develop integrated and coordinated strategies to incorporate survivorship care plans into the electronic medical record specifically and more broadly within cancer centers [25].

Fig. 1 Changes in knowledge and behavior from baseline to 6 months. The intervention effectively improved knowledge of healthy diet, physical activity, and dietary supplement use at 3 months of follow-up, and the effect on healthy diet knowledge persisted at 6 months. P values <0.05 are displayed. The intervention also significantly reduced the

frequency of alcohol intake at 3 months. In addition, we found that the intervention was more effective in improving knowledge of healthy diet and dietary supplement and increasing frequency of physical activities in non-Hispanic whites than in Hispanics at 3 months

J Cancer Surviv (2016) 10:956–963 961

The primary strengths of the study are the randomized, single-blinded, and prospective nature of the trial and the het- erogeneity of the study population. In addition, we measured changes in multiple domains related to behavior change, in- cluding attitudes, knowledge, and actual behaviors. A limita- tion is that an educational intervention was used in both arms, and therefore, the intervention was not compared to usual care. It is possible that both are better than usual care. Additional limitations are that comprehensive standardized measures of diet and physical activity were not used, and we did not account for multiple comparisons in our analyses. Future studies should use standardized behavior assessments to quantify the effects of survivorship care plans on changes in diet and physical activity.

Compared with standard NCI-issued written survivor- ship materials, a 2-h survivorship intervention (1 h with nurse and 1 h with nutritionist) was associated with short-term increased knowledge of lifestyle recommen- dations, change in physical activity, and change in die- tary behaviors among a multi-ethnic group of breast cancer survivors. The intervention was more effective in non-Hispanics compared to Hispanics, suggesting that interventions may need to be tailored to cultural and socioeconomic factors. Behavioral effects were not ob- served beyond 3 months. A single lifestyle consultation is likely not enough to achieve and maintain lifestyle recommendations. Currently, more comprehensive models changing lifestyle behaviors in the survivorship setting are being tested, particularly related to diet, physical activity, and weight maintenance (e.g., NCI R01 CA186080, PI: H Greenlee; Alliance 011401 PI: Ligibel). These studies will provide information on what supports are needed to effectively achieve and maintain behavior change among diverse populations of breast cancer survivors. To facilitate long-term behavioral change among breast cancer survivors in the adjuvant setting, culturally competent behavioral interventions are likely needed to increase knowledge of and the ca- pabilities needed to meet lifestyle recommendations.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict of interest.

Ethical approval All procedures performed in studies involving hu- man participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Funding This study was funded by Susan G. Komen for The Cure DISP0706868 (DLH), the Breast Cancer Research Foundation (DLH), and National Institutes of Health National Cancer Institute K23CA141052 (HG) and NCI R25T CA094061-12 (CSM).

Informed consent Informed consent was obtained from all individual participants included in the study.

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