Impact of a Tailored Nutrition and Lifestyle Intervention for Overweight Cancer Survivors on Dietary Patterns, Physical Activity, Quality of Life, and Cardiometabolic Profiles

Colleen K Spees, Ashlea C Braun, Emily B Hill, Elizabeth M Grainger, James Portner, Gregory S Young, Matthew D Kleinhenz, Chureeporn Chitchumroonchokchai, Steven K Clinton, Colleen K Spees, Ashlea C Braun, Emily B Hill, Elizabeth M Grainger, James Portner, Gregory S Young, Matthew D Kleinhenz, Chureeporn Chitchumroonchokchai, Steven K Clinton

Abstract

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. The 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. The 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, and the mean age was 58 years. Compared to baseline, participants had significant improvements in Healthy Eating Index (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 (-3.9 kg), waist circumference (-5.5 cm), BMI (-1.5 kg/m2), systolic BP (-9.5 mmHg), plasma carotenoids (+35%), total cholesterol (-6%), triglycerides (-14%), hs-CRP (-28%), and IGFBP-3 (-5%) (all p < 0.010). These 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. This trial is registered on ClinicalTrials.gov NCT02268188.

Conflict of interest statement

The authors declare that there are no conflicts of interest regarding the publication of this paper.

Copyright © 2019 Colleen K. Spees et al.

References

    1. Miller K. D., Siegel R. L., Lin C. C., et al. Cancer treatment and survivorship statistics, 2016. CA: A Cancer Journal for Clinicians. 2016;66(4):271–289. doi: 10.3322/caac.21349.
    1. Carver J. R., Shapiro C. L., Ng A., et al. American Society of Clinical Oncology clinical evidence review on the ongoing care of adult cancer survivors: cardiac and pulmonary late effects. Journal of Clinical Oncology. 2007;25(25):3991–4008. doi: 10.1200/jco.2007.10.9777.
    1. Playdon M. C., Bracken M. B., Sanft T. B., Ligibel J. A., Harrigan M., Irwin M. L. Weight gain after breast cancer diagnosis and all-cause mortality: systematic review and meta-analysis. Journal of the National Cancer Institute. 2015;107(12):p. djv275. doi: 10.1093/jnci/djv275.
    1. Min Park S., Kyung Lim M., Won Jung K., et al. Prediagnosis smoking, obesity, insulin resistance, and second primary cancer risk in male cancer survivors: national health insurance corporation study. Journal of Clinical Oncology. 2007;25(30):4835–4843. doi: 10.1200/jco.2006.10.3416.
    1. Spark L. C., Reeves M. M., Fjeldsoe B. S., Eakin E. G. Physical activity and/or dietary interventions in breast cancer survivors: a systematic review of the maintenance of outcomes. Journal of Cancer Survivorship. 2013;7(1):74–82. doi: 10.1007/s11764-012-0246-6.
    1. Hoedjes M., van Stralen M. M., Joe S. T. A., et al. Toward the optimal strategy for sustained weight loss in overweight cancer survivors: a systematic review of the literature. Journal of Cancer Survivorship. 2017;11(3):360–385. doi: 10.1007/s11764-016-0594-8.
    1. World Cancer Research Fund/American Institute for Cancer Research. London, UK: World Cancer Research Fund/American Institute for Cancer Research; 2018. Diet, nutrition, physical activity and cancer: a global perspective. Continue Update Project Expert Report.
    1. Kushi L. H., Doyle C., McCullough M., et al. American Cancer Society guidelines on nutrition and physical activity for cancer prevention. CA: A Cancer Journal for Clinicians. 2012;62(1):30–67. doi: 10.3322/caac.20140.
    1. US Department of Health and Human Services and US Department of Agriculture. 2015–2020 Dietary Guidelines for Americans. 8th. Washington, DC, USA: US Department of Health and Human Services and US Department of Agriculture; 2015.
    1. Kohler L. N., Garcia D. O., Harris R. B., Oren E., Roe D. J., Jacobs E. T. Adherence to diet and physical activity cancer prevention guidelines and cancer outcomes: a systematic review. Cancer Epidemiology Biomarkers & Prevention. 2016;25(7):1018–1028. doi: 10.1158/1055-9965.epi-16-0121.
    1. Elwood P. C., Whitmarsh A., Gallacher J., et al. Healthy living and cancer: evidence from UK biobank. Ecancermedicalscience. 2018;12(792) doi: 10.3332/ecancer.2018.792.
    1. Stacey F. G., James E. L., Chapman K., Courneya K. S., Lubans D. R. A systematic review and meta-analysis of social cognitive theory-based physical activity and/or nutrition behavior change interventions for cancer survivors. Journal of Cancer Survivorship. 2015;9(2):305–338. doi: 10.1007/s11764-014-0413-z.
    1. US Department of Health and Human Services. National Heart, Lung, and Blood Institute, Lifestyle Work Group. Lifestyle Interventions to Reduce Cardiovascular Risk: Systematic Evidence Review from the Lifestyle Work Group. Bethesda, MA, USA: National Institutes of Health; 2013.
    1. Eckel R. H., Jakicic J. M., Ard J. D., et al. AHA/ACC guideline on lifestyle management to reduce cardiovascular risk: a report of the American college of cardiology/American heart association task force on practice guidelines. Journal of the American College of Cardiology. 2014;63:2960–2984.
    1. Spees C. K., Hill E. B., Grainger E. M., et al. Feasibility, preliminary efficacy, and lessons learned from a garden-based lifestyle intervention for cancer survivors. Cancer Control. 2016;23(3):302–310. doi: 10.1177/107327481602300314.
    1. Janssen H., Ada L., Bernhardt J., et al. An enriched environment increases activity in stroke patients undergoing rehabilitation in a mixed rehabilitation unit: a pilot non-randomized controlled trial. Disability and Rehabilitation. 2014;36(3):255–262. doi: 10.3109/09638288.2013.788218.
    1. Lambert K., Hyer M., Bardi M., et al. Natural-enriched environments lead to enhanced environmental engagement and altered neurobiological resilience. Neuroscience. 2016;330:386–394. doi: 10.1016/j.neuroscience.2016.05.037.
    1. Morton L. W., Bitto E. A., Oakland M. J., Sand M. Accessing food resources: rural and urban patterns of giving and getting food. Agriculture and Human Values. 2008;25:107–119.
    1. Park S.-A., Lee A.-Y., Lee H.-S., Lee K.-S., Son K.-C. A comparison of exercise intensity between two horticultural and four common physical activities among male adults in their 20s. Korean Journal of Horticultural Science and Technology. 2015;33(1):133–142. doi: 10.7235/hort.2015.14084.
    1. Soga M, Gaston KJ, Yamaura Y. Gardening is beneficial for health: a meta-analysis. Preventive Medicine Reports. 2016;5:92–99.
    1. Pérez-Escamilla R., Obbagy J. E., Altman J. M., et al. Dietary energy density and body weight in adults and children: a systematic review. Journal of the Academy of Nutrition and Dietetics. 2012;112(5):671–684. doi: 10.1016/j.jand.2012.01.020.
    1. Blair C. K., Madan-Swain A., Locher J. L., et al. Harvest for health gardening intervention feasibility study in cancer survivors. Acta Oncologica. 2013;52(6):1110–1118. doi: 10.3109/0284186x.2013.770165.
    1. Demark-Wahnefried W., Cases M. G., Cantor A. B., et al. Pilot randomized controlled trial of a home vegetable gardening intervention among older cancer survivors shows feasibility, satisfaction, and promise in improving vegetable and fruit consumption, reassurance of worth, and the trajectory of central adiposity. Journal of the Academy of Nutrition and Dietetics. 2018;118(4):689–704. doi: 10.1016/j.jand.2017.11.001.
    1. Rock C. L., Flatt S. W., Byers T. E., et al. Results of the exercise and nutrition to enhance recovery and good health for you (ENERGY) trial: a behavioral weight loss intervention in overweight or obese breast cancer survivors. Journal of Clinical Oncology. 2015;33(28):3169–3176. doi: 10.1200/jco.2015.61.1095.
    1. McCarroll M. L., Armbruster S., Frasure H. E., et al. Self-efficacy, quality of life, and weight loss in overweight/obese endometrial cancer survivors (SUCCEED): A randomized controlled trial. Gynecologic Oncology. 2014;132(2):397–402. doi: 10.1016/j.ygyno.2013.12.023.
    1. Focht B. C., Lucas A. R., Grainger E., et al. Effects of a group-mediated exercise and dietary intervention in the treatment of prostate cancer patients undergoing androgen deprivation therapy: results from the Idea-P trial. Annals of Behavioral Medicine. 2018;52(5):412–428. doi: 10.1093/abm/kax002.
    1. Hartmann C., Dohle S., Siegrist M. A self-determination theory approach to adults’ healthy body weight motivation: a longitudinal study focussing on food choices and recreational physical activity. Psychology & Health. 2015;30(8):924–948. doi: 10.1080/08870446.2015.1006223.
    1. Spees C. K., Joseph A., Darragh A., Lyons F., Wolf K. N. Health behaviors and perceptions of cancer survivors harvesting at an urban garden. American Journal of Health Behavior. 2015;39(2):257–266. doi: 10.5993/ajhb.39.2.12.
    1. Ligibel J. A., Denlinger C. S. New NCCN guidelines for survivorship care. Journal of the National Comprehensive Cancer Network. 2013;11(5S):640–644. doi: 10.6004/jnccn.2013.0191.
    1. McCabe M. S., Bhatia S., Oeffinger K. C., et al. American Society of Clinical Oncology statement: achieving high-quality cancer survivorship care. Journal of Clinical Oncology. 2013;31(5):631–640. doi: 10.1200/jco.2012.46.6854.
    1. Braun A., Portner J., Grainger E. M., et al. Tele-motivational interviewing for cancer survivors: feasibility, preliminary efficacy, and lessons learned. Journal of Nutrition Education and Behavior. 2018;50(1):19–32. doi: 10.1016/j.jneb.2017.05.352.
    1. Kraus W. E., Janz K. F., Powell K. E., et al. Daily step counts for measuring physical activity exposure and its relation to health. Medicine & Science in Sports & Exercise. 2019;51(6):1206–1212. doi: 10.1249/mss.0000000000001932.
    1. US Department of Health and Human Services. Physical Activity Guidelines for Americans. 2nd. Washington, DC, USA: US Department of Health and Human Services; 2018.
    1. Armstrong M. J., Mottershead T. A., Ronksley P. E., Sigal R. J, Campbell T. S, Hemmelgarn B. R. Motivational interviewing to improve weight loss in overweight and/or obese patients: a systematic review and meta-analysis of randomized controlled trials. Obesity Reviews: An Official Journal of the International Association for the Study of Obesity. 2011;12:709–723. doi: 10.1111/j.1467-789X.2011.00892.x.
    1. Burgess E., Hassmén P., Welvaert M., Pumpa K. L. Behavioural treatment strategies improve adherence to lifestyle intervention programmes in adults with obesity: a systematic review and meta-analysis. Clinical Obesity. 2017;7(2):105–114. doi: 10.1111/cob.12180.
    1. Karnes S. L., Meyer B. B., Berger L. M., Brondino M. J. Changes in physical activity and psychological variables following a web-based motivational interviewing intervention: pilot study. JMIR Research Protocols. 2015;4(4):p. e129. doi: 10.2196/resprot.4623.
    1. Guenther P. M., Kirkpatrick S. I., Reedy J., et al. The Healthy Eating Index-2010 is a valid and reliable measure of diet quality according to the 2010 Dietary Guidelines for Americans. The Journal of Nutrition. 2014;144(3):399–407. doi: 10.3945/jn.113.183079.
    1. Miller P. E., Mitchell D. C., Harala P. L., Pettit J. M., Smiciklas-Wright H., Hartman T. J. Development and evaluation of a method for calculating the healthy eating index-2005 using the nutrition data System for research. Public Health Nutrition. 2011;14(2):306–313. doi: 10.1017/s1368980010001655.
    1. Mayne S. T., Cartmel B., Scarmo S., et al. Noninvasive assessment of dermal carotenoids as a biomarker of fruit and vegetable intake. The American Journal of Clinical Nutrition. 2010;92(4):794–800. doi: 10.3945/ajcn.2010.29707.
    1. Cooperstone J. L., Ralston R. A., Riedl K. M., et al. Enhanced bioavailability of lycopene when consumed ascis-isomers fromtangerinecompared to red tomato juice, a randomized, cross-over clinical trial. Molecular Nutrition & Food Research. 2015;59(4):658–669. doi: 10.1002/mnfr.201400658.
    1. Ferrell B. R., Hassey Dow K., Grant M. Measurement of the quality of life in cancer survivors. Quality of Life Research. 1995;4(6):523–531. doi: 10.1007/bf00634747.
    1. Centers for Disease Control and Prevention. BRFSS Questionnaires. Behavioral Risk Factor Surveillance System. Atlanta, GA, USA: Centers for Disease Control and Prevention; 2016.
    1. Eikenberry N., Smith C. Healthful eating: perceptions, motivations, barriers, and promoters in low-income Minnesota communities. Journal of the American Dietetic Association. 2004;104(7):1158–1161. doi: 10.1016/j.jada.2004.04.023.
    1. Chen G., Gully S. M., Eden D. Validation of a new general self-efficacy scale. Organizational Research Methods. 2001;4(1):62–83. doi: 10.1177/109442810141004.
    1. Cox M., Basen-Engquist K., Carmack C. L., et al. Comparison of internet and telephone interventions for weight loss among cancer survivors: randomized controlled trial and feasibility study. JMIR Cancer. 2017;3(2):p. e16. doi: 10.2196/cancer.7166.
    1. Koutoukidis D. A., Beeken R. J., Manchanda R., et al. Recruitment, adherence, and retention of endometrial cancer survivors in a behavioural lifestyle programme: the Diet and Exercise in Uterine Cancer Survivors (DEUS) parallel randomised pilot trial. BMJ Open. 2017;7 doi: 10.1136/bmjopen-2017-018015.e018015
    1. James E. L., Stacey F. G., Chapman K., et al. Impact of a nutrition and physical activity intervention (ENRICH: exercise and Nutrition Routine Improving Cancer Health) on health behaviors of cancer survivors and carers: a pragmatic randomized controlled trial. BMC Cancer. 2015;15:p. 710. doi: 10.1186/s12885-015-1775-y.
    1. Deshmukh A. A., Shirvani S. M., Likhacheva A., Chhatwal J., Chiao E. Y., Sonawane K. The association between dietary quality and overall and cancer-specific mortality among cancer survivors, NHANES III. JNCI Cancer Spectrum. 2018;2(2) doi: 10.1093/jncics/pky022.pky022
    1. Schwingshackl L., Bogensberger B., Hoffmann G. Diet quality as assessed by the healthy eating index, alternate healthy eating index, dietary approaches to stop hypertension score, and health outcomes: an updated systematic review and meta-analysis of cohort studies. Journal of the Academy of Nutrition and Dietetics. 2018;118(1):74–100. doi: 10.1016/j.jand.2017.08.024.
    1. Reedy J., Krebs-Smith S. M., Miller P. E, et al. Higher diet quality is associated with decreased risk of all-cause, cardiovascular disease, and cancer mortality among older adults. The Journal of Nutrition. 2014;144(6):881–889. doi: 10.3945/jn.113.189407.
    1. Zhang F. F., Liu S., John E. M., Must A., Demark-Wahnefried W. Diet quality of cancer survivors and noncancer individuals: results from a national survey. Cancer. 2015;121(23):4212–4221. doi: 10.1002/cncr.29488.
    1. Wang Y., Chen X. Between-group differences in nutrition- and health-related psychosocial factors among US adults and their associations with diet, exercise, and weight status. Journal of the Academy of Nutrition and Dietetics. 2012;112(4):486–498. doi: 10.1016/j.jand.2011.12.003.
    1. Burrows T. L., Williams R., Rollo M., et al. Plasma carotenoid levels as biomarkers of dietary carotenoid consumption: a systematic review of the validation studies. Journal of Nutrition & Intermediary Metabolism. 2015;2(1-2):15–64. doi: 10.1016/j.jnim.2015.05.001.
    1. Wang X., Ouyang Y., Liu J., et al. Fruit and vegetable consumption and mortality from all causes, cardiovascular disease, and cancer: systematic review and dose-response meta-analysis of prospective cohort studies. BMJ. 2014;349:p. g4490. doi: 10.1136/bmj.g4490.
    1. Kahleova H., Tura A., Hill M., Holubkov R., Barnard N. A plant-based dietary intervention improves beta-cell function and insulin resistance in overweight adults: a 16-week randomized clinical trial. Nutrients. 2018;10(2):p. 189. doi: 10.3390/nu10020189.
    1. Berentzen T. L., Jakobsen M. U., Halkjaer J., et al. Changes in waist circumference and mortality in middle-aged men and women. PLoS One. 2010;5 doi: 10.1371/journal.pone.0013097.e13097
    1. Simon M. S., Beebe-Dimmer J. L., Hastert T. A., et al. Cardiometabolic risk factors and survival after breast cancer in the Women’s Health Initiative. Cancer. 2018;124(8):1798–1807. doi: 10.1002/cncr.31230.
    1. Kritchevsky S. B., Beavers K. M., Miller M. E., et al. Intentional weight loss and all-cause mortality: a meta-analysis of randomized clinical trials. PLoS One. 2015;10 doi: 10.1371/journal.pone.0121993.e0121993
    1. Garcia M. T., Ribeiro S. M., Germani A. C. C. G., Bógus C. M. The impact of urban gardens on adequate and healthy food: a systematic review. Public Health Nutrition. 2018;21(2):416–425.
    1. Zhou Y., Irwin M. L., Ferrucci L. M., et al. Health-related quality of life in ovarian cancer survivors: results from the American cancer society’s study of cancer survivors–I. Gynecologic Oncology. 2016;141(3):543–549. doi: 10.1016/j.ygyno.2016.04.006.
    1. Hamer J., Warner E. Lifestyle modifications for patients with breast cancer to improve prognosis and optimize overall health. Canadian Medical Association Journal. 2017;189(7):E268–E274. doi: 10.1503/cmaj.160464.
    1. Samdal G. B., Eide G. E., Barth T., Williams G., Meland E. Effective behaviour change techniques for physical activity and healthy eating in overweight and obese adults; systematic review and meta-regression analyses. International Journal of Behavioral Nutrition and Physical Activity. 2017;14:p. 42. doi: 10.1186/s12966-017-0494-y.
    1. Spencer J. C., Wheeler S. B. A systematic review of Motivational Interviewing interventions in cancer patients and survivors. Patient Education and Counseling. 2016;99(7):1099–1105. doi: 10.1016/j.pec.2016.02.003.
    1. Smits A., Lopes A., Das N., Bekkers R., Massuger L., Galaal K. The effect of lifestyle interventions on the quality of life of gynaecological cancer survivors. Gynecologic Oncology. 2015;139(3):546–552. doi: 10.1016/j.ygyno.2015.10.002.
    1. Travier N., Buckland G., Vendrell J. J., et al. Changes in metabolic risk, insulin resistance, leptin and adiponectin following a lifestyle intervention in overweight and obese breast cancer survivors. European Journal of Cancer Care. 2018;27 doi: 10.1111/ecc.12861.e12861

Source: PubMed

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