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Hindawi Journal of Oncology Volume 2019, Article ID 1503195, 13 pages https://doi.org/10.1155/2019/1503195 Research Article Impact of a Tailored Nutrition and Lifestyle Intervention for Overweight Cancer Survivors on Dietary Patterns, Physical Activity, Quality of Life, and Cardiometabolic Profiles 1,2 1 1 2,3 Colleen K. Spees , Ashlea C. Braun, Emily B. Hill, Elizabeth M. Grainger, 4 5 6 James Portner, Gregory S. Young , Matthew D. Kleinhenz, 3 2,3 Chureeporn Chitchumroonchokchai, and Steven K. Clinton Medical Dietetics & Health Sciences, School of Health and Rehabilitation Sciences, e Ohio State University College of Medicine, Columbus, Ohio, USA Comprehensive Cancer Center, e Ohio State University, Columbus, Ohio, USA Department of Internal Medicine, Division of Medical Oncology, e Ohio State University, Columbus, Ohio, USA College of Social Work, e Ohio State University, Columbus, Ohio, USA Center for Biostatistics, e Ohio State University, Columbus, Ohio, USA Department of Horticulture and Crop Science, e Ohio State University, Columbus, Ohio, USA Correspondence should be addressed to Colleen K. Spees; spees.11@osu.edu Received 21 June 2019; Revised 9 September 2019; Accepted 5 October 2019; Published 21 November 2019 Guest Editor: Demosthenes Panagiotakos Copyright © 2019 Colleen K. Spees et al. *is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Survivors of cancer often experience treatment-related toxicity in addition to being at risk of cancer recurrence, second primary cancers, and greater all-cause mortality. *e objective of this study was to test the safety and efficacy of an intensive evidence-based garden intervention to improve outcomes for cancer survivors after curative therapy. To do so, a clinical trial of adult overweight and obese cancer survivors within 2 years of completing curative therapy was completed. *e 6-month intervention, delivered within the context of harvesting at an urban garden, combined group education with cooking demonstrations, remote motivational interviewing, and online digital resources. Data on dietary patterns, program satisfaction, and quality of life were collected via questionnaires; anthropometrics, physical activity, and clinical biomarkers were measured objectively. Of the 29 participants, 86% were white, 83% were female,andthemean agewas58years. Comparedtobaseline, participantshad significantimprovements inHealthyEatingIndex (HEI) scores (+5.2 points, p � 0.006), physical activity (+1,208 steps, p � 0.033), and quality of life (+16.07 points, p � 0.004). Significant improvements were also documented in weight (− 3.9kg), waist circumference (− 5.5cm), BMI (− 1.5kg/m ), systolic BP (− 9.5mmHg), plasma carotenoids (+35%), total cholesterol (− 6%), triglycerides (− 14%), hs-CRP (− 28%), and IGFBP-3 (− 5%) (all p<0.010). *ese findings demonstrate a tailored multifaceted garden-based biobehavioral intervention for overweight and obese cancer survivors after curative therapy is safe and highly effective, warranting larger randomized controlled trials to identify program benefits, optimal maintenance strategies, program value relative to cost, and approaches for integration into a survivor’s oncology management program. *is trial is registered on ClinicalTrials.gov NCT02268188. health comorbidities, in addition to those present at di- 1. Introduction agnosis [2]. Moreover, over 60% of cancer survivors in the Advances in cancer diagnosis and treatment have led to a U.S. are considered overweight or obese, increasing the risk greater proportion of patients achieving a complete re- of additional cancers and sequelae of metabolic syndrome, mission and durable cure [1]. However, survivors face a reduced physical functioning, and all-cause mortality [3, 4]. multitude of short- and long-term physical and mental Cancer survivors also experience health issues secondary to 2 Journal of Oncology adherence as compared with nongarden-based approaches, the rigors of cancer therapy associated with surgical in- terventions, radiation, and chemotherapeutics, disrupting yet few garden studies have specifically targeted overweight and obese cancer survivors [15, 22, 23]. nutritional status, physical function, and metabolism [1]. We currently lack evidence from studies integrating diet, Aligning with the evidence-based guidelines, our tai- nutrition, and physical activity for cancer survivors dem- lored intervention was designed to achieve higher compli- onstrating long-term improvement in health outcomes ance than past dietary and fitness interventions for cancer [5, 6]. *us, standard of care nutrition and physical activity survivors and improvements in metrics of health and QOL programs are not routinely integrated into oncology care, a and dietary and physical activity patterns [23–25]. Our problem compounded by financial barriers, such as lack of intensive intervention was previously evaluated to assess feasibility and preliminary efficacy prior to proceeding to the coverage by insurance programs. Organizations including the World Cancer Research Fund/American Institute for development of a larger randomized intervention compared with standards of care [15]. In the current study, our ob- Cancer Research (WCRF/AICR) have formulated evidence- based cancer prevention guidelines focused on maintaining jective was to determine the safety and efficacy of the in- tervention after adapting it to meet the unique needs of a healthy body weight, physical fitness, and a primarily plant-based dietary pattern [7, 8]. Expert committees and overweight and obese cancer survivors. We hypothesized clinicians advise cancer survivors to follow public health our intervention would be successfully adapted to this guidelines (e.g., the Dietary Guidelines for Americans and population of survivors and demonstrate safety and efficacy. the WCRF/AICR recommendations) in the absence of more precise programs [7–11]. 2. Materials and Methods *eory-driven approaches addressing multiple lifestyle behaviors in cancer survivors have demonstrated promise, 2.1. Participants. Recruitment was conducted in local on- yet there remains a need to develop and evaluate a more cology clinics, community centers, and other communica- effective intervention, both in the proportion of individuals tion channels targeting survivors. Participants were English- responding and the degree of change, than current standards speaking survivors (≥18 years) who completed active cancer and define biobehavioral strategies that enhance outcomes treatment within the previous 48 months (current adjuvant and promote maintenance [12]. More recently, a greater hormone therapy was acceptable), currently without evi- appreciation exists for individual variation in response to dence of active cancer, and a body mass index (BMI)≥25kg/ behavioral programs, and future success depends upon the m . Participants were ineligible if they were cognitively development of tailored interventions. Increasingly, reviews unable to consent; participating in recent or ongoing diet of relevant interventions to improve health outcomes have and exercise programs; diagnosed with conditions pre- concluded standard, formulaic approaches show modest cluding physical activity; consuming medications with di- short-term efficacy, but poor long-term success [13, 14]. *e etary contraindications (e.g., warfarin); unwilling to ongoing challenge is to define, implement, and evaluate discontinue nonprescribed supplements, herbals, or bo- tailored lifestyle programs targeting high-risk subgroups tanicals; diagnosed with significant metabolic or digestive such as those with overweight or obesity, amongst others. disorders, renal or hepatic insufficiency, cachexia, and short We have previously developed an integrated in- bowel syndrome; or pregnant [15]. All study procedures tervention strategy, and the current study presents an ad- were approved by the Institutional Review Board at *e aptation to this strategy to target overweight and obese Ohio State University. All participants provided written cancer survivors. Described in detail elsewhere, our com- informed consent. prehensive, theory-driven intervention combines group and tailored individual education coupled with an enriched environment in hopes of promoting social stimulation, 2.2.Intervention. *is trial was designed to assess the safety group support, behavior change, and self-management to and efficacy of a novel and intensive multifaceted lifestyle elicita significantresponseincardiometabolicoutcomes and intervention for overweight or obese adult cancer survivors. quality of life (QOL) [15]. Evidence in human and animal Informed by a feasibility pilot in nonobese survivors, we models highlights the potential for cognitive and social further refined and expanded our program to integrate stimulation in low-stakes settings to promote beneficial tailored components, including multiple biobehavioral tools psychological effects, including modulation of neuro- with documented value in previous work for specialized plasticity, particularly those that are natural versus manu- support [14, 15, 26]. A greater emphasis was placed on factured (e.g., characterized by vegetation) [16, 17]. theoretical aspects for education to encourage autonomy in Furthermore, active participation in gardening has been selecting avenues for improving adherence to cancer pre- documented to increase the quantity and variety of produce vention guidelines, including group and one-on-one in- consumed while increasing physical activity and functional teractions addressing knowledge gaps while facilitating the status comparably to other moderate-intensity activities transformation of targeted information to tailored goals [18–20]. Increased consumption of produce has been linked [14, 26, 27]. In brief, the 6-month intervention components to displacement of calories and energy-dense foods, which included (1) weekly urban garden experiences and har- can contribute to weight loss [21]. Preliminary studies vesting (fruits, vegetables, and herbs) [28]; (2) semimonthly suggest garden-based interventions targeting those with group education classes, each including a 30-minute in- nutrition-related chronic disease demonstrate improved teractive discussion surrounding evidence-based guidelines; Journal of Oncology 3 guidelines, including displacementof calories by shiftingtoa (3) semimonthly cooking demonstrations, complementing group education and using produce harvested from the primarily plant-based dietary pattern. study garden to encourage incorporation into meals and to provide opportunities for taste testing [7, 8, 29, 30]; (4) 2.2.3. Cooking Demonstrations. To encourage utilization of remote motivational interviewing coaching (tele-MI) [31]; garden produce and provide opportunities for skill devel- and (5) supportive technologies, including a pedometer to opment, each group education session was coupled with an track steps and access to a secure web portal with multiple interactive cooking demonstration provided by a medical functions. center chef and RD. Lasting approximately 30 minutes, each Collectively, the intervention was designed to encourage demonstration included descriptions and hands-on exam- achievement of numerous participant-level goals; throughout, ples to reinforce basic cooking and food preparation tech- registered dietitians(RDs) promotedpersonal goalsettingand niques (e.g., knife skills). Recipes prepared incorporated empowerment to adopt and sustain positive behavior change. available produce from the study garden to empower par- A primary objective of the program was to foster the adoption ticipants to utilize these skills to prepare similar meals and of a primarily plant-based dietary pattern in order to displace snacks at home. calories from energy-dense sources. Participants were en- couragedtofollowrecommendationsfromthe2015-2020U.S. Dietary Guidelines for Americans as well as those specifically 2.2.4. Motivational Interviewing. In order to provide tai- outlined in cancer survivor-specific recommendations and lored support while maximizing intrinsic motivation, an RD achieve a daily 500-calorie deficit [7–9]. In addition, partic- served as the tele-MI coach for this intervention after ap- ipants were encouraged to achieve the recommendations set propriate training [31]. Well-defined and implemented MI forth by the Physical Activity Guidelines for Americans (e.g., has proven efficacious in various settings and populations 150 minutes of moderate-intensity exercise per week, or [34, 35]. MI has been implemented in interventions utilizing 10,000 steps per day); these two goals combined to contribute remote platforms as a mechanism for behavior change; thus, toaweightlossofapproximatelyonepoundperweek[32,33]. methods for interacting with the tele-MI coach in this in- tervention were chosen by each participant (e.g., email, text, and telephone) during the course of the study [36]. In brief, 2.2.1. Garden Experience. A key principle of this in- each participant was contacted within one week of their tervention was the integration of an enriched environment baseline assessment, with weekly contacts attempted into the program with the goal of enhancing the efficacy and thereafter. Each correspondence was based on individual impact on physical and mental health outcomes. Accord- goals and served to assist participants in addressing barriers, ingly, our integrated and enriched garden-based in- overcoming ambivalence, or otherwise supporting indi- tervention included harvesting fresh garden produce one to vidual needs; all tele-MI interactions remained separate three times per week. *is intervention component offered from study-related reminders. *e MI methodology has participants the opportunity to derive both cognitive and been previously reported [31]. social stimulation. To further optimize the enriched envi- ronment, the study components were offered in a supportive and relaxed manner, allowing for flexibility in participation 2.2.5. Supportive Technologies. To supplement the educa- of some components (e.g., optional tele-MI). tional material covered in the education classes, participants *e garden was a 3-acre plot integrated within a 261-acre were provided with access to a secure web portal which agricultural research farm on the university campus, staffed housed cancer survivor-specific information, additional for this study with RDs and horticulture students. *e resources, and electronic copies of handouts and recipes garden was planted to offer a wide variety of produce over from classes. Updated weekly, the website housed links to the growing season. Adjacent to the garden is an indoor external websites and information on the benefits of the university classroom equipped for cooking demonstrations. available garden produce. Participants were encouraged to At enrollment, participants were oriented to farm policies, utilize the website when missing a class or if more in- safety issues, and harvesting techniques and provided a formation was required. Participants were also encouraged harvest bag and registration card to electronically track to weigh themselves and submit logs to the secure web portal participation. weekly. *is remote tracking was reviewed by the tele-MI coach, who created individual and de-identified group 2.2.2. Group Education. Study participants attended faculty- graphical records depicting change over time, allowing guided group education sessions every two weeks. Each 30- participants to view individual and group progress to minute session focused on at least one of the evidence-based stimulate continued participation. *e tele-MI coach also recommendations, including those relating to dietary and provided additional information, including links to educa- tional materials and evidence-based resources. physical activity patterns, and was facilitated by a local expert and included an interactive question and answer *e overarching goal of our intervention was to achieve greater compliance with the evidence-based guidelines session [7, 9]. While delivering targeted information for cancer survivors, these sessions served to provide partici- coupled with greater impact on biomarkers than previous pants information they needed to encourage and empower dietary and fitness interventions for cancer survivors [7, 9]. them to adopt a diet consistent with evidence-based *erefore, our objectives were to improve participant (1) 4 Journal of Oncology weight; (2) dietary patterns; (3) physical activity patterns; (4) including physical well-being, psychological well-being, QOL; and (5) relevant biomarkers of health. social concerns, and spiritual well-being. Additional per- sonal, health, and behavioral information were collected via modified Behavioral Risk Factor Surveillance System 2.3. Data Collection (BRFSS) questions and additional questions to assess mo- tivation [42, 43]. Self-efficacy was assessed via the New 2.3.1. Dietary Patterns. Participants at baseline and post- General Self-Efficacy scale and additional study-specific interventionreportedtheirconsumptionoffoodandbeverages questions to assess participant confidence in adhering to over 30 days using the VioScreen Graphical Food Frequency evidence-based guidelines [44]. Questionnaire (FFQ, Viocare, Inc., Princeton, NJ). *is al- gorithm-driven, computer-delivered FFQ uses the Nutrition Data System for Research database (Nutrition Coordinating 2.3.5. Program Evaluation. Following completion of the Center, University of Minnesota) for analysis. Diet quality was intervention, participants were provided a comprehensive assessed using Healthy Eating Index 2010 (HEI), which questionnaire to provide feedback on the program, in- measures compliance with the U.S. Dietary Guidelines for cluding each of its components. *ese include closed- and Americans [37]. *ese scores were automatically tabulated by open-ended questions to elicit both quantitative indicators VioScreen utilizing previously described methods [38]. of participants’ perceptions as well as qualitative data. 2.3.2.PhysicalActivityPatterns. Givenlowbaselinelevels,our 2.4. Statistical Analyses. Statistical analyses for the effect of physical activity goal was modest, focusing on daily steps. the intervention on anthropometric, dietary, and clinical Participants received pedometers (Omron Healthcare Co. Inc., measures compared the baseline and postintervention LakeForest,IL)whichservedtomotivateandreinforcebehavior values, testing the null hypothesis of no change in these change, as well as for data collection. Participants reviewed their variables usingpairedt-tests.Values for lipids, inflammatory daily steps and uploaded numbers weekly to the secure web markers, and plasma carotenoids were log transformed prior portal. *e tele-MI coach also reviewed these data and provided to analysis due to heteroscedasticity. For these outcomes, graphical tracking records to show change over time. differences from baseline to postintervention were expressed as fold-change. For evaluation of compliance, participations were considered compliant if they attended/utilized≥75% of 2.3.3. Clinical and Laboratory Measurements. Participants the in-person education sessions and/or related remote completed laboratory visits at baseline and postintervention components. All analyseswere performedin SPSS version 23 following a 12-hour fast and 72-hour period of avoidance of (SPSS Inc, Chicago, IL) or SAS v9.4 (SAS Institute, Cary, vigorous exercise or alcohol consumption. Visits were con- NC). ducted between 7:00am and 10:00am. Participants were weighed wearing light clothing and no shoes on a calibrated Pro Plus digital scale (Health-o-Meter Professional Products, 3. Results Pelstar LLC, Bridgeview, IL) to the nearest 0.1kg. Height was 3.1. Recruitment, Retention, and Baseline Characteristics. measured using a calibrated stadiometer (Health-o-Meter A total of 56 adult cancer survivors were screened for eli- Professional Products, Pelstar LLC, Bridgeview, IL) to the gibility, and 35 (n �28 female, n �7 male) were deemed nearest1mm.*reewaistcircumference(WC)measurements eligible and enrolled. During the study, 2 were removed due were obtained between the costal margin and the iliac crest to to cancer recurrence, 1 withdrew due to a noncancer health the nearest 1mm. Blood pressure was obtained using an issue, and 3 due to personal issues. No grade 3 or 4 adverse OmronAutocuff(OmronHealthcareCo.Ltd.,LakeForest,IL) events were documented based upon Common Terminology standardized against a manual sphygmomanometer. Skin Criteria for Adverse Events (v4.0). Of the final cohort carotenoid levels were assessed noninvasively with a Phar- (n �29), the majority were white and female (86.2% and manex Nu Skin BioPhotonic Scanner S3 (Nu Skin Enterprises, 82.8%, respectively, Table 1). *e mean age was 58.0 years, Provo, UT), utilizing resonance Raman spectroscopy [39]. and the mean age of initial cancer diagnosis was 52.9 years Venous blood samples were obtained by trained phle- for females and 65.2 years for males. Breast (44.8% of total, botomistswith20mLofbloodintoVacutainer tubes(Becton, 54.2% of females) and prostate (17.2% of total, 100% of Dickinson and Co., Franklin Lakes, NJ). EDTA Vacutainer males) cancers were the most prevalent primary cancers. tubes were used forcarotenoid profiling by a high performance liquid chromatography-diode array detector following pre- viously developed methods [40]. Blood samples were imme- 3.2.AttendanceandAdherence. Compliance with each of the diately processed for lipid profiles, hemoglobin A1c (HbA1c), multiple components of the intervention was high. On av- adiponectin, insulin, leptin, and inflammatory markers hs- erage, participants attended 90% (9/10) of the education CRP, IGF-1, and IGFBP-3 using standard protocols. sessions, and mean class attendance was 24 of 29 participants (84%). Individually, participants attended 15 of 25 weeks of 2.3.4. Quality of Life and Other Behaviors. *e Quality of harvest (59%), with greater attendance on weeks when edu- Life Patient/Cancer Survivor Version (QOL-CSV) [41] cation sessions were scheduled. All participants submitted questionnaire was used to estimate perceived health pedometer steps, with 15 of 29 participants (52%) completing Journal of Oncology 5 Table1: Demographicsand characteristics ofoverweightcancersurvivors participating ina 6-monthbehavioralinterventionstudy (n �29). Participant characteristics Valid % (n) Age (years) 58.0 Female 82.8 (24) Sex Male 17.2 (5) White/Caucasian 86.2 (25) Race/ethnicity Black/African American 10.3 (3) Asian 3.4 (1) Married 62.1 (18) Divorced 13.8 (4) Marital status Never married 13.8 (4) Others 10.3 (3) Less than grade 12/grade 12 equivalent 10.3 (3) College 1 to 3 years 10.3 (3) Education College 4 years or more 44.8 (13) Professional or graduate 34.5 (10) Employed or self-employed 51.7 (15) Employment Retired 44.8 (13) Out of work<1 year 3.4 (1) >$50,000 51.7 (15) Household income $10,000–$49,999 27.6 (8) Prefer not to answer/do not know 20.7 (6) Female 52.9 Primary cancer diagnosis (age, years) Male 65.2 Breast 44.8 (13) Prostate 17.2 (5) Primary cancer Ovarian/uterine 13.8 (4) Colorectal 6.9 (2) Others 17.3 (5) Data are presented as % and n and include baseline characteristics of participants that completed both baseline and postintervention data collection visits. a b Percentage based upon the number of participants for whom data was available. Widowed, separated, member of an unmarried couple, or prefer not to answer. Lymphoma (10.3%), brain (3.4%), and pancreatic (3.4%). whole fruit (+0.6, p � 0.009), fatty acids (+1.5, p � 0.007), every week of the 6-month intervention, while 26 of 29 (90%) submitted step data for at least 80% of the weeks. Twenty-six refined grains (+1.1, p � 0.013), and empty calories (+2.1, participants (90%) reported use of the secure web portal, and p � 0.008) also improved; scores for total vegetables trended 59% of participants utilized tele-MI. For individual commu- positively (+0.4, p � 0.054). nication, participants requested use of email (n=14, 48.3%), Carotenoid status, which served as a biomarker of phone (n=3, 10.3%), text message (n=2, 6.9%), or mixed produce intake, increased from pre- to postintervention. preferences/no preference (n=10, 34.5%). In total, 71% of Total dietary carotenoid intakes increased by 66% interactionsoccurredviae-mailwhile57%ofparticipantsused (p<0.001), including increases in individual intakes of all 5 telephonic interactions and 10% used text messages, described major carotenoids consumed in the diet (data not presented in more detail elsewhere [31]. here). Likewise, total plasma carotenoids improved signifi- cantly (+35%, p<0.001, Table 3) as did several individual carotenoids (e.g., alpha-carotene p<0.001, total beta-car- 3.3. Dietary and Physical Activity Patterns. Participants otene p<0.001, total lycopene p � 0.017). Skin carotenoids improved their adherence to the dietary and physical activity also increased over the course of the intervention evidence-based guidelines for cancer survivorship. Aligning (p � 0.015) and demonstrated a strong, positive correlation with weight loss goals, participants demonstrated improve- with total plasma carotenoids (r �0.73, p<0.001). ments in measures of dietary intakes, including a decrease in Compared with baseline, participants increased their daily mean energy intake (− 250kcal, p � 0.012), an increase physical activity patterns to more closely align with evi- in vegetable and fruit consumption (+1.05 servings, p<0.001 dence-based guidelines. Indeed, mean steps per day in- and +0.41 servings, p � 0.022, respectively), and a decrease in creased from 6,560 to 7,768 (+18.9%, p � 0.033) over the consumption of added sugars (− 2.37 tsp., p � 0.036) from course of the intervention. baseline to postintervention (data not presented here). In- creasesindietqualitybaseduponsignificantimprovementsof HEI scores from baseline to postintervention are shown in 3.4. Anthropometric and Clinical Measures. Changes in Table 2. Total diet scores improved by 5.2 points on a 100- anthropometric measures and clinical indicators are de- pointscale(p � 0.006).Scoresfortotalfruit(+0.8, p � 0.003), tailed in Table 3. Significant reductions were noted in body 6 Journal of Oncology Table 2: Change in Healthy Eating Index scores in overweight cancer survivors participating in a 6-month behavioral intervention study (n �29). HEI component Max score Baseline Postintervention Mean difference (95% CI) Unadjusted p value Adequacy (higher score indicates higher consumption) Total diet 100 69.6±12.3 74.8±9.8 +5.2 (1.6, 8.8) 0.006 Total fruit 5 3.6±1.5 4.4±1.1 +0.8 (0.3, 1.3) 0.003 Whole fruit 5 4.2±1.3 4.8±0.7 +0.6 (0.2, 1.0) 0.009 Total vegetables 5 4.5±0.9 4.9±0.4 +0.4 (− 0.01, 0.7) 0.054 Greens and beans 5 4.3±1.2 4.6±1.0 +0.3 (− 0.2, 0.7) 0.307 Whole grains 10 5.9±3.6 5.7±3.5 − 0.2 (− 1.2, 0.7) 0.607 Dairy 10 7.5±2.3 6.8±2.9 − 0.7 (− 1.6, 0.1) 0.082 Total protein foods 5 4.7±0.5 4.4±1.0 − 0.3 (− 0.6, 0.1) 0.170 e,f Seafood and plant proteins 5 4.3±1.0 4.5±0.9 +0.2 (− 0.1, 0.5) 0.148 g ∗ Fatty acids 10 4.7±3.0 6.2±3.2 +1.5 (0.5, 2.6) 0.007 Moderation (higher score indicates lower consumption) Refined grains 10 8.7±2.2 9.8±0.7 +1.1 (0.3, 2.0) 0.013 Sodium 10 2.7±2.8 2.3±2.9 − 0.4 (− 1.7, 0.8) 0.449 h ∗ Empty calories 20 14.4±4.3 16.5±3.9 +2.1 (0.6, 3.6) 0.008 Data are presented as mean±standard deviation, and changes are expressed as mean differences for participants that completed both baseline and postintervention assessment visits. Data are Healthy Eating Index 2010 (HEI) scores for participants that completed both baseline and postintervention assessments. HEI is a scoring metric that assesses diet quality as specified by the US Dietary Guidelines for Americans [37]. It is made up of 12 components: 9 for adequacy and 3 for moderation. A higher score indicates better conformance to dietary guidance, and the total HEI score is the sum of the component a b c scores. HEI, Healthy Eating Index. Includes 100% fruit juice. Includes all forms except juice. Includes any beans and peas not counted toward total protein d e foods. Includes all milk products, such as fluid milk, yogurt, and cheese, and fortified soy beverages. Beans and peas are included here (not with vegetables) when the total protein foods standard is otherwise not met. Includes seafood, nuts, seeds, and soy products (other than beverages) as well as beans and peas g h counted as total protein foods. Ratio of poly- and monounsaturated fatty acids (PUFAs and MUFAs) to saturated fatty acids (SFAs). Calories from solid fats, alcohol, and added sugars; threshold for counting alcohol is >28g/day. p<0.05. Table 3: Change in anthropometric and clinical biomarkers in overweight cancer survivors participating in a 6-month behavioral in- tervention study (n �29). Variable Baseline Postintervention Mean difference or fold change (95% CI) Unadjusted p value Weight (kg) 85.3±16.2 81.4±16.7 − 3.9 (− 5.6, − 2.2) <0.001 Body mass index (kg/m ) 31.9±5.1 30.4±5.3 − 1.5 (− 2.1, − 0.8) <0.001 Waist circumference (cm) 102.0±13.6 96.5±13.6 − 5.5 (− 6.9, − 4.1) <0.001 Systolic BP (mmHg) 127.7±15.8 118.1±13.0 − 9.5 (− 16.0, − 3.0) 0.006 Diastolic BP (mmHg) 75.0±8.3 73.2±8.0 − 1.8 (− 4.7, 1.0) 0.197 HbA1c (%) 5.7±0.5 5.7±0.5 0.0 (− 0.3, 0.3) 0.879 a ∗ Total cholesterol (mg/dL) 190.4±29.5 179.2±32.2 0.94 (0.90, 0.98) 0.004 HDL (mg/dL) 54.9±13.3 53.4±13.0 0.97 (0.92, 1.03) 0.275 LDL (mg/dL) 113.5±28.6 107.7±29.0 0.95 (0.89, 1.00) 0.052 Triglycerides (mg/dL) 133.2±52.7 113.1±44.4 0.86 (0.76, 0.96) 0.010 a ∗ hs-CRP (mg/L) 4.0±4.2 3.3±4.1 0.72 (0.58, 0.89) 0.004 IGFBP-3 (μg/mL) 4.7±0.9 4.5±0.8 0.95 (0.91, 0.98) 0.005 IGF-1 (ng/mL) 95.6±34.1 104.5±40.1 1.07 (0.86, 1.33) 0.553 Leptin (ng/mL) 35.7±33.0 29.4±28.7 0.71 (0.40, 1.26) 0.226 Adiponectin (µg/mL) 12.9±87.3 13.0±71.9 1.06 (0.76, 1.47) 0.740 Insulin (pg/mL) 490.7±310.9 459.6±253.2 0.97 (0.72, 1.30) 0.821 Total skin carotenoids (RRS counts) 29,509±11,471 33,963±14,441 4,455 (944, 7,965) 0.015 Total plasma carotenoids (nmoL/L) 1,749.5±871.7 2,330.0±1220.8 1.35 (1.15, 1.58) <0.001 a,b Lutein+zeaxanthin (nmoL/L) 98.7±60.0 125.3±84.1 1.27 (0.98, 1.64) 0.066 Beta-cryptoxanthin (nmoL/L) 143.71±162.4 121.1±76.1 1.02 (0.82, 1.27) 0.840 Alpha-carotene (nmoL/L) 140.7±95.2 293.5±263.6 1.91 (1.52, 2.40) <0.001 a ∗ Beta-carotene all-trans (nmoL/L) 603.8±507.1 884.5±676.0 1.56 (1.22, 2.01) 0.001 Beta-carotene–cis (nmoL/L) 65.7±38.9 78.2±39.1 1.29 (1.03, 1.62) 0.028 a ∗ Total beta-carotene (nmoL/L) 669.5±539.3 962.7±711.8 1.50 (1.21, 1.86) <0.001 Lycopene all-trans (nmoL/L) 526.7±257.5 601.9±244.6 1.20 (0.99, 1.44) 0.060 Lycopene–cis (nmoL/L) 189.5±116.1 247.7±112.4 1.46 (1.12, 1.89) 0.006 Total lycopene (nmoL/L) 716.2±361.9 849.6±336.7 1.26 (1.05, 1.53) 0.017 Data are presented as mean±standard deviation, and changes are expressed as mean differences or fold change for participants that completed both baseline and postintervention assessment visits. BP, blood pressure; HbA1c, hemoglobin A1c; HDL, high-density lipoprotein; LDL, low-density lipoprotein; hs-CRP, high-sensitivity C-reactive protein; IGFBP-3, insulin-like growth factor-binding protein-3; IGF-1, insulin-like growth factor 1. Log transformed prior to b ∗ analysis and difference expressed as fold change. All plasma zeaxanthin values below detectable limit. p<0.05. Journal of Oncology 7 Table 4: Change in select quality of life scores in overweight cancer survivors participating in a 6-month behavioral intervention study (n �29). Item Baseline Postintervention Mean difference (95% CI) Unadjusted p value Quality of life (total score) 268.86±51.24 284.93±51.75 +16.07 (5.5, 26.6) 0.004 Physical well-being Fatigue 5.59±2.64 6.52±2.72 +0.93 (0.01, 1.86) 0.049 Appetite changes 7.93±2.42 8.14±2.25 +0.21 (− 0.76, 1.17) 0.664 Sleep changes 6.79±2.57 7.17±2.35 +0.38 (− 0.60, 1.36) 0.436 Constipation 8.52±2.25 8.07±2.51 − 0.45 (− 1.19, 0.29) 0.223 Please rate your overall physical health 6.24±2.12 7.10±1.47 +0.86 (− 0.05, 1.77) 0.062 Psychological well-being How good is your quality of life? 7.17±2.27 8.28±1.22 +1.10 (0.18, 2.03) 0.021 How much happiness do you feel? 7.59±1.52 7.79±1.47 +0.21 (− 0.33, 0.74) 0.432 Do you feel like you are in control of things in your 7.10±2.04 7.45±1.76 +0.34 (− 0.31, 1.00) 0.289 life? How satisfying is your life? 7.48±1.84 7.86±1.43 +0.38 (− 0.17, 0.93) 0.170 How useful do you feel? 7.21±2.14 7.76±1.81 +0.55 (0.06, 1.05) 0.030 To what extent are you fearful of: Future diagnostic tests 5.38±3.11 6.45±2.43 +1.07 (0.06, 2.08) 0.039 A second cancer 5.72±2.93 6.66±2.91 +0.93 (− 0.06, 1.92) 0.064 Recurrence of your cancer 4.79±3.06 5.83±3.35 +1.03 (0.09, 1.98) 0.033 Spreading (metastasis) of your cancer 5.31±3.42 6.48±3.29 +1.17 (0.16, 2.18) 0.025 Social concerns Is the amount of support you receive from others 8.00±2.55 7.79±2.51 − 0.21 (− 0.96, 0.55) 0.580 sufficient to meet your needs? To what degree has your illness and treatment 6.93±3.34 8.59±2.13 +1.66 (0.66, 2.65) 0.002 interfered with your employment? How much isolation do you feel is caused by your 8.00±2.58 8.10±2.76 +0.10 (− 0.45, 0.65) 0.703 illness or treatment? Spiritual well-being How much has your spiritual life changed as a result 5.17±3.35 5.93±3.23 +0.76 (− 0.61, 2.13) 0.266 of your cancer diagnosis? To what extent has your illness made positive changes 5.72±2.76 6.48±2.68 +0.76 (0.06, 1.45) 0.033 in your life? Do you sense a purpose/mission for your life or a 6.86±2.30 7.48±2.47 +0.62 (− 0.10, 1.34) 0.089 reason for being alive? How hopeful do you feel? 7.69±1.61 8.28±1.69 +0.59 (0.15, 1.02) 0.010 Data are presented as mean±standard deviation, and changes are expressed as mean differences for participants that completed both baseline and postintervention assessment visits. Data were obtained using the Quality of Life Patient/Cancer Survivor Version (QOL-CSV), including subscales for physical, psychological, social, and spiritual well-being. Select responses from each subscale are presented. For all items, an increase in score indicates an improvement in QOL. p<0.05. weight (− 3.9kg), BMI (− 1.5kg/m ), WC (− 5.5cm), total prevention guidelines; data not presented here). Participants cholesterol (TC) (− 6%), systolic BP (− 9.5mmHg), and reported taking fewer medications and supplements at triglycerides (TG) (− 14%). Analysis of inflammatory postintervention (prescribed and over-the-counter), with markers revealed significant decreases in hs-CRP and fewer challenges associated with eating healthy. Specifically, IGFBP-3 (by 28%, p � 0.004 and 5%, p � 0.005, re- fewer participants described barriers related to cost, dislike of healthy food, knowledge regarding preparation and what spectively) as well as decreases in insulin levels (by 3%), though these failed to reach significance. Participant logged constitutes healthy food, access, desire, ease of purchase, and weights demonstrate consistent moderate weight loss willpower. throughout the intervention (Supplementary Figure 1). 3.6.AcceptabilityofIntervention. Participants reported high 3.5. Qualitative Measures. Overall QOL significantly im- acceptability of the intervention (Table 5). Ninety-three proved (+16.07 points, p � 0.004) as well as several subscales percent rated both the program and harvesting as “excellent” indicating improvements in physical, psychological, and or “very good.” Amongst all components, participants rated spiritual well-being, characterized by fewer feelings of dis- the group education sessions most effective (55%), followed tress secondary to illness and treatment, as well as cancer- by harvesting (34%) and tele-MI (18% of those that utilized). related fears (Table 4). Positive trends were noted in total Participants reported the program impacted their overall self-efficacy (+3%, p � 0.061), with stronger findings health in a positive manner (97%), provided them with a amongst study-specific items (i.e., adherence to cancer sense of community and support (93%), and stated they 8 Journal of Oncology Table 5: Acceptability of intervention in overweight cancer survivors participating in a 6-month behavioral intervention study (n �29). Survey questions Responses % (n) Would you recommend this program to other Yes 96.6 (28) survivors? No 3.4 (1) Excellent 72.4 (21) Very good 20.7 (6) How would you rate the program as a whole? Good 6.9 (2) Fair 0.0 (0) Poor 0.0 (0) Excellent 58.6 (17) Very good 34.5 (10) How would you rate the group educational classes? Good 3.4 (1) Fair 3.4 (1) Poor 0.0 (0) Excellent 55.2 (16) Very good 37.9 (11) How would you rate the harvesting at the garden? Good 6.9 (2) Fair 0.0 (0) Poor 0.0 (0) Excellent 58.8 (10) How would you rate the individualized coaching Very good 29.4 (5) (one-on-one with tele-motivational interviewing Good 11.8 (2) coaching)? Fair 0.0 (0) Poor 0.0 (0) Group education 55.2 (16) Which program activity was most effective for you? Harvesting produce 34.5 (10) Please pick only one. Health coaching 17.6 (3) Did the program impact your overall health in a Yes 96.6 (28) positive manner? No 3.4 (1) Did the program help you to achieve better dietary Yes 96.6 (28) patterns that more closely align with the cancer survivor recommendations (primarily plant-based, No 3.4 (1) rich in whole grains, fruits, and vegetables and low in sodium, simple sugars, and red/processed meats)? Did the program help you to improve your physical Yes 93.1 (27) activity patterns to more closely align with the cancer survivor recommendations (150 minutes of moderate No 6.9 (2) physical activity/week or 10,000 steps/day)? Did the program provide you with a sense of Yes 93.1 (27) community and support? No 6.9 (2) Do you plan to continue to use the information you Yes 100.0 (29) received as part of the program to make decisions No 0.0 (0) regarding your health? Data are presented as % and n. Data presented are from program-specific evaluation questions asked of participants at postintervention assessment visits. Tele-motivational interviewing coaching percentage based upon those that utilized the coaching. would recommend the program to other survivors (97%). safe and effective interventions to reverse these risks and Twenty-eight participants (97%) agreed the program helped promote heath and QOL. To date, while numerous in- them achieve better dietary patterns, and 27 participants terventions have been designed for cancer survivors and have (93%) agreed the program helped them improve their shown modest success, tailored programs with individualized physical activity patterns. Based on program evaluation, all support are few and further are not standardized or fully participants (100%, n �29) planned to use the information integrated into cancer care, similar to cardiac rehabilitation gleaned to make future health-related decisions. models [12]. *e development of such programs and data to demonstrate the safety, efficacy, and value (cost/impact) derived from well-designed and rigorous clinical trials is 4. Discussion critical. *ose programs showing promise can move forward Obesity, metabolic syndrome, declines in physical fitness, and into randomized multi-institutional studies in comparison their sequelae are common in cancer survivors [1]. Coupled with the current standards of care, which are minimal. with additional risks of chronic toxicities and complications *e objective of this study was to evaluate the safety and from cancer therapies, it is imperative survivors have access to efficacy of our multicomponent intervention adapted to a Journal of Oncology 9 *esedietarychangesarereflectiveofdisplacementofenergy- population of overweight and obese cancer survivors, with the overarching goal of this intervention being improved dense, nutrient-depleted, and highly processed foods for nutrient- and phytochemical-rich options, which also con- adherence to the evidence-based guidelines. *e recruitment goals were met, and the present cohort was similar with tributes to calorie reductions. respect to age, sex, and sociodemographic profiles to those in Other clinical biomarkers, including inflammatory in- comparable lifestyle interventions for cancer survivors, and dicators and those related to cardiometabolic health, also the cancer diagnoses of those recruited were similar to those improved after the intervention, consistent with other be- frequently targeted [45]; our cohort included a higher havioral interventions promoting primarily plant-based percentage of females due to the strong breast cancer dietary patterns [55]. *e present study resulted in signif- icant improvements in weight, BMI, WC, systolic BP, TC, program at our institution. *e retention and participation was higher than previously reported studies of diet/lifestyle TG, and hs-CRP. Specifically, participants achieved a sus- tainable weight loss of approximately 0.25kg (>0.5 pounds) interventions in cancer survivors [46]. Indeed, attrition from the trial was just over 15%, with the major issues for per week over the 24 weeks of the study in parallel with increases in physical activity by nearly 20%. Furthermore, withdrawal or removal being travel, vacations, and disease recurrence. Safety of the intervention is supported by the WC decreased 5%, translating into a 9%decreased risk of all- absence of grade 3 and 4 adverse events based upon cause mortality and decrease in cardiovascular disease risk Common Terminology Criteria for Adverse Events (v4.0). [56, 57]. In participants who were obese at baseline, the Participation in the key components of the intervention, intentional weight loss is associated with a 15% decrease in including lectures and cooking demonstrations (84% at- all-cause mortality risk and is further associated with a tendance), garden harvesting (84% during weeks with class, reduction in cardiometabolic risk in cancer survivors [58]. Leptin and adiponectin trended positively, though these 59% on off-weeks), pedometer utilization (90%), web-based utilization (90%), and tele-MI (59%) was high. We attribute measures generally demonstrate great variability among individuals and our study lacked sufficient power to detect such high retention and participation rates to the tailored and flexible approach coupled with the intensity and fre- significant changes. *ese data, taken together, support the conclusion that this intervention, based upon energy bal- quency of contact, leading to greater improvements in key outcomes compared to those reported elsewhere [47]. ance, dietary patterns, and fitness, has the potential if sus- Participants indicated the program helped them better tained to have significant cardioprotective benefits. align their lifestyle behaviors with the evidence-based A recent systematic review documents the emerging lit- guidelines for cancer survivorship, a finding which was erature regarding garden-based interventions, indicating collectively reinforced by positive outcomes in self-report changes in beliefs, knowledge, and attitudes surrounding measures, objective indices of health, and clinical biomarkers. healthy food, as well as improvements in healthy food practices (e.g., variety of produce consumed), while high- Assessments of dietary patterns indicated participants more closely aligned with a plant-based dietary pattern at post- lighting the need for assessment of objective biomarkers of health [59]. Emerging thematic patterns suggest potential intervention [7–9]. *is improvement is potentially conse- quential if sustained, as recent analyses of national cancer value of integration of enriched environment experiences survivor outcomes demonstrated high diet quality is associ- within strategies for behavior change. While challenging to atedwithasubstantialreductioninoverallandcancer-specific measure, the data presented here demonstrate this, with mortality, leading authors to conclude that high-quality diets participants reporting significant improvements in QOL and may protect against death among survivors [48, 49]. In ad- indices of health, including physical, psychological, and dition to improved intakes of specific food groups, the study spiritual well-being. In comparison, studies of cancer survi- cohort’s HEI improvement of >5 points translates into an vors document a decrease in general QOL, including mea- estimated 5% decrease in mortality when compared to a sures of mental and physical well-being, social functioning, vitality, pain, and capacities to fulfill physical and emotional similarly aged population [50].Itis importantto note the total HEI score for the study cohort was 22 points higher at roles one to two years after diagnosis [60]. *e high com- pliance in participation and impact on measured outcomes is baseline than the total HEI score documented for cancer survivors across the U.S. [51]. *is finding is likely due to likely, in part, due to the social networking that occurs with healthier survivors being more likely to commit to a diet and the shared garden experience [61]. Indeed, 93% reported both exercise program coupled with higher income, greater formal a sense of community and an overall positive impression of education, and Caucasian race, all characteristics of trial the garden experience. We can speculate the instructive and participants [52]. Nonetheless, these findings were mirrored natural environment may have contributed to improvements by increases in skin and plasma carotenoids, which serve as a in biomarkers of health. Evidence in animal models has demonstrated such natural environments can similarly elicit quantitative biomarker associated with reported produce intakes [39, 53]. *e increased plasma concentrations of improvements in emotional health and neurobiological re- sponses contributing to behavioral modifications, such as multiple individual carotenoids demonstrated increased consumption of a variety of fruits and vegetables [53]. Evi- shifts in motivation [17]. It is plausible the combination of a mentoredgarden experiencewithhands-onlearningactivities dence that dietary patterns high in fruits and vegetables and modest in intakes of sodium, added sugar, and saturated fat (e.g., cooking demonstrations) may have rendered similar are inversely related to cardiovascular disease, and all-cause benefits. Coupled with cooking demonstrations, the garden mortality informs the guidelines for cancer survivors [7, 54]. experience effectively introduced new varieties of produce, 10 Journal of Oncology behaviors than nonparticipants. *is may contribute to altered previous taste preferences, encouraged adventurous eating, modified perceptions regarding cost and availability, higher baseline values (e.g., HEI); however, the documented improvement over time challenges this, as well as con- and taught new preparation techniques. Our experience suggests that MI can contribute to in- comitant improvement in biological values, which have dividual success by emphasizing autonomy, addressing previously shown to correlate to self-reported outcomes ambivalence, and promoting intrinsic motivation through [15]. *e results of this work warrant continued research to ongoing one-on-one support. In line with previous be- elucidate the relationship between psychological and bi- havioral research, the incorporation of MI as one compo- ological outcomes. nent of a multicomponent lifestyle intervention can promote long-term changes in health outcomes, including weight 5. Conclusions loss, improved dietary patterns, and increases in physical activity, in both the general population and in cancer sur- We have demonstrated high compliance and impact of a vivors [34, 35, 62, 63]. Results from program evaluations multifaceted but fully integrated and tailored program indicated that 18% of tele-MI users perceived it as the most targeting dietary and physical activity patterns, weight, and effective component ofthe intervention.Whilenotranked as cardiometabolic outcomes in cancer survivors. Most criti- the most effective intervention component overall, these cally, the inclusion of tele-MI and a garden experience likely results suggest that for a percentage of participants, MI is contributed significantly to the improvement of multiple beneficial. We believe that a multifaceted intervention which quantified outcomes, including QOL. To better assess this encourages participants to engage in various components is impact, future studies must emphasize long-term mainte- empowering and promotes success. In this cohort, greater nance. In parallel, large-scale studies comparing this pro- weight loss (4.8 vs. 2.6kg) and improvements in QOL gram to standards of care, including evaluation of the costs (p � 0.030), amongst other variables, were observed with and potential benefits for cancer survivors as well as future utilization of tele-MI [31]. healthcare utilization, are necessary. *ese key studies may We report a multidisciplinary and highly integrated allow for a cancer survivor program to be fully integrated garden-based intervention that significantly improved di- into cancer care similarly to cardiac rehabilitation strategies, etary and physical activity patterns, as well as clinical and now considered standard of care and reimbursed by payers. laboratory markers of health in overweight and obese cancer survivors. *e program employs multiple tools for tailoring Data Availability the intervention for individuals, integrating feedback and support mechanisms, and promoting behavior change *e data used to support the findings of this study are through evidence-based core curriculum, all of which is available from the corresponding author upon request. provided to cancer survivors in a low-pressure enriched garden environment. As a culmination of theory-driven Conflicts of Interest techniques previously shown to result in clinically relevant outcomes as well as those capable of improving QOL, these *e authors declare that there are no conflicts of interest components work in concert to provide flexibility while regarding the publication of this paper. enhancing intrinsic motivation, commitment to change, and overall well-being [64, 65]. Our strategy going forward is to continue to integrate a portfolio of options during an in- Acknowledgments tervention suited to individual needs, based upon unique life *e authors thank Glenn Mills, Director, Waterman Agri- schedules, computer/technical savvy, education and back- cultural and Natural Resources Laboratory Operations; grounds, and comorbidities, yet all integrated within a Anna Marconi, Program Coordinator and Horticulture uniform evidence-based dietary and fitness program. Outreach Specialist, Waterman Agricultural and Natural Although caution remains in the interpretation of a Resources Laboratory Operations; and JamesCare for Life. single-arm study, the main value is demonstrating an in- *is work was supported by the American Cancer Society. tervention with high retention and impact. *us, random- ized, large-scale studies are critical to test the ability to implement this effort and compare with standards of care. Supplementary Materials Limitations include the absence of a control group and the small size and homogeneity of the final cohort, all of which Figure 1: self-reported change in weight (mean kg) in limit the generalizability of our results. *e few participants overweight cancer survivors participating in a 6-month who withdrew from the study speak to limitations secondary behavioral intervention study. Participants weighed them- to participants’ inability to maintain attendance in the selves daily and logged weights via an online secure web context of personal challenges, such as transportation. portal. Weekly means were based on the number of par- Amongst those who completed the intervention and in ticipants each week. Group data were shown at education whom positive results were documented, there is the pos- sessions to demonstrate progress and motivate participants. sibility these advantageous outcomes were the result of the Weights were not logged for week 0 or week 24 due to Hawthorne effect. In addition, the “healthy participant” baseline and postintervention clinic visits. (Supplementary effect may be present, in which participants report healthier Materials) Journal of Oncology 11 association task force on practice guidelines,” Journal of the References American College of Cardiology, vol. 63, pp. 2960–2984, 2014. [1] K. D. Miller, R. L. Siegel, C. C. 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Published: Nov 21, 2019
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