Randomized controlled trial to evaluate the effects of combined progressive exercise on metabolic syndrome in breast cancer survivors: rationale, design, and methods

Christina M Dieli-Conwright, Joanne E Mortimer, E Todd Schroeder, Kerry Courneya, Wendy Demark-Wahnefried, Thomas A Buchanan, Debu Tripathy, Leslie Bernstein, Christina M Dieli-Conwright, Joanne E Mortimer, E Todd Schroeder, Kerry Courneya, Wendy Demark-Wahnefried, Thomas A Buchanan, Debu Tripathy, Leslie Bernstein

Abstract

Background: Metabolic syndrome (MetS) is increasingly present in breast cancer survivors, possibly worsened by cancer-related treatments, such as chemotherapy. MetS greatly increases risk of cardiovascular disease and diabetes, co-morbidities that could impair the survivorship experience, and possibly lead to cancer recurrence. Exercise has been shown to positively influence quality of life (QOL), physical function, muscular strength and endurance, reduce fatigue, and improve emotional well-being; however, the impact on MetS components (visceral adiposity, hyperglycemia, low serum high-density lipoprotein cholesterol, hypertriglyceridemia, and hypertension) remains largely unknown. In this trial, we aim to assess the effects of combined (aerobic and resistance) exercise on components of MetS, as well as on physical fitness and QOL, in breast cancer survivors soon after completing cancer-related treatments.

Methods/design: This study is a prospective randomized controlled trial (RCT) investigating the effects of a 16-week supervised progressive aerobic and resistance exercise training intervention on MetS in 100 breast cancer survivors. Main inclusion criteria are histologically-confirmed breast cancer stage I-III, completion of chemotherapy and/or radiation within 6 months prior to initiation of the study, sedentary, and free from musculoskeletal disorders. The primary endpoint is MetS; secondary endpoints include: muscle strength, shoulder function, cardiorespiratory fitness, body composition, bone mineral density, and QOL. Participants randomized to the Exercise group participate in 3 supervised weekly exercise sessions for 16 weeks. Participants randomized to the Control group are offered the same intervention after the 16-week period of observation.

Discussion: This is the one of few RCTs examining the effects of exercise on MetS in breast cancer survivors. Results will contribute a better understanding of metabolic disease-related effects of resistance and aerobic exercise training and inform intervention programs that will optimally improve physiological and psychosocial health during cancer survivorship, and that are ultimately aimed at improving prognosis.

Trial registration: NCT01140282;

Registration: June 10, 2010.

Figures

Figure 1
Figure 1
Study design. Endpoints are assessed at baseline (T1), after the end of the 16-week intervention (T2), and 12 weeks post-intervention (Exercise Group only; T3).
Figure 2
Figure 2
Study flow.

References

    1. Ries L, Melbert D, Krapcho M, Mariotto A, Miller BA, Feuer EJ, Clegg L, Horner MJ, Howlader N, Eisner MP, Reichman M, Edwards BK, editor. SEER Cancer Statistics review, 1975–2004. Bethesda, MD: National Cancer Institute; 2006.
    1. Hewitt M, Rowland JH, Yancik R. Cancer survivors in the United States: age, health, and disability. J Gerontol A Biol Sci Med Sci. 2003;58(1):82–91. doi: 10.1093/gerona/58.1.M82.
    1. Holmes MD, Chen WY, Feskanich D, Kroenke CH, Colditz GA. Physical activity and survival after breast cancer diagnosis. JAMA. 2005;293(20):2479–2486. doi: 10.1001/jama.293.20.2479.
    1. Irwin ML, Crumley D, McTiernan A, Bernstein L, Baumgartner R, Gilliland FD, Kriska A, Ballard-Barbash R. Physical activity levels before and after a diagnosis of breast carcinoma: the health, eating, activity, and lifestyle (HEAL) study. Cancer. 2003;97(7):1746–1757. doi: 10.1002/cncr.11227.
    1. Irwin ML, Smith AW, McTiernan A, Ballard-Barbash R, Cronin K, Gilliland FD, Baumgartner RN, Baumgartner KB, Bernstein L. Influence of pre- and postdiagnosis physical activity on mortality in breast cancer survivors: the health, eating, activity, and lifestyle study. J Clin Oncol. 2008;26(24):3958–3964. doi: 10.1200/JCO.2007.15.9822.
    1. Cadmus LA, Salovey P, Yu H, Chung G, Kasl S, Irwin ML. Exercise and quality of life during and after treatment for breast cancer: results of two randomized controlled trials. Psychooncology. 2009;18(4):343–352. doi: 10.1002/pon.1525.
    1. Twiss JJ, Waltman NL, Berg K, Ott CD, Gross GJ, Lindsey AM. An exercise intervention for breast cancer survivors with bone loss. J Nurs Scholarsh. 2009;41(1):20–27. doi: 10.1111/j.1547-5069.2009.01247.x.
    1. Bower JE, Ganz PA, Desmond KA, Rowland JH, Meyerowitz BE, Belin TR. Fatigue in breast cancer survivors: occurrence, correlates, and impact on quality of life. J Clin Oncol. 2000;18(4):743–753.
    1. Burgess C, Cornelius V, Love S, Graham J, Richards M, Ramirez A. Depression and anxiety in women with early breast cancer: five year observational cohort study. BMJ. 2005;330(7493):702. doi: 10.1136/bmj.38343.670868.D3.
    1. Irwin ML, McTiernan A, Baumgartner RN, Baumgartner KB, Bernstein L, Gilliland FD, Ballard-Barbash R. Changes in body fat and weight after a breast cancer diagnosis: influence of demographic, prognostic, and lifestyle factors. J Clin Oncol. 2005;23(4):774–782. doi: 10.1200/JCO.2005.04.036.
    1. Hack TF, Pickles T, Ruether JD, Weir L, Bultz BD, Mackey J, Degner LF. Predictors of distress and quality of life in patients undergoing cancer therapy: impact of treatment type and decisional role. Psychooncology. 2009;19(6):606–616. doi: 10.1002/pon.1590.
    1. Courneya KS, Mackey JR, Bell GJ, Jones LW, Field CJ, Fairey AS. Randomized controlled trial of exercise training in postmenopausal breast cancer survivors: cardiopulmonary and quality of life outcomes. J Clin Oncol. 2003;21(9):1660–1668. doi: 10.1200/JCO.2003.04.093.
    1. Irwin ML, Varma K, Alvarez-Reeves M, Cadmus L, Wiley A, Chung GG, Dipietro L, Mayne ST, Yu H. Randomized controlled trial of aerobic exercise on insulin and insulin-like growth factors in breast cancer survivors: the yale exercise and survivorship study. Cancer Epidemiol Biomarkers Prev. 2009;18(1):306–313. doi: 10.1158/1055-9965.EPI-08-0531.
    1. Ohira T, Schmitz KH, Ahmed RL, Yee D. Effects of weight training on quality of life in recent breast cancer survivors: the weight training for breast cancer survivors (WTBS) study. Cancer. 2006;106(9):2076–2083. doi: 10.1002/cncr.21829.
    1. Schmitz KH, Ahmed RL, Troxel A, Cheville A, Smith R, Lewis-Grant L, Bryan CJ, Williams-Smith CT, Greene QP. Weight lifting in women with breast-cancer-related lymphedema. N Engl J Med. 2009;361(7):664–673. doi: 10.1056/NEJMoa0810118.
    1. Kushi LH, Doyle C, McCullough M, Rock CL, Demark-Wahnefried W, Bandera EV, Gapstur S, Patel AV, Andrews K, Gansler T. American cancer society guidelines on nutrition and physical activity for cancer prevention: reducing the risk of cancer with healthy food choices and physical activity. CA Cancer J Clin. 2012;62(1):30–67. doi: 10.3322/caac.20140.
    1. Bernstein L, Henderson BE, Hanisch R, Sullivan-Halley J, Ross RK. Physical exercise and reduced risk of breast cancer in young women. J Natl Cancer Inst. 1994;86(18):1403–1408. doi: 10.1093/jnci/86.18.1403.
    1. McTiernan A, Kooperberg C, White E, Wilcox S, Coates R, Adams-Campbell LL, Woods N, Ockene J. Recreational physical activity and the risk of breast cancer in postmenopausal women: the Women’s health initiative cohort study. JAMA. 2003;290(10):1331–1336. doi: 10.1001/jama.290.10.1331.
    1. Morey MC, Snyder DC, Sloane R, Cohen HJ, Peterson B, Hartman TJ, Miller P, Mitchell DC, Demark-Wahnefried W. Effects of home-based diet and exercise on functional outcomes among older, overweight long-term cancer survivors: RENEW: a randomized controlled trial. JAMA. 2009;301(18):1883–1891. doi: 10.1001/jama.2009.643.
    1. Knobf MT, Insogna K, DiPietro L, Fennie C, Thompson AS. An aerobic weight-loaded pilot exercise intervention for breast cancer survivors: bone remodeling and body composition outcomes. Biol Res Nurs. 2008;10(1):34–43. doi: 10.1177/1099800408320579.
    1. Segal R, Evans W, Johnson D, Smith J, Colletta S, Gayton J, Woodard S, Wells G, Reid R. Structured exercise improves physical functioning in women with stages I and II breast cancer: results of a randomized controlled trial. J Clin Oncol. 2001;19(3):657–665.
    1. De Backer IC, Van Breda E, Vreugdenhil A, Nijziel MR, Kester AD, Schep G. High-intensity strength training improves quality of life in cancer survivors. Acta Oncol. 2007;46(8):1143–1151. doi: 10.1080/02841860701418838.
    1. Courneya KS, Segal RJ, Mackey JR, Gelmon K, Reid RD, Friedenreich CM, Ladha AB, Proulx C, Vallance JK, Lane K, Yasui Y, McKenzie DC. Effects of aerobic and resistance exercise in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial. J Clin Oncol. 2007;25(28):4396–4404. doi: 10.1200/JCO.2006.08.2024.
    1. McKenzie DC, Kalda AL. Effect of upper extremity exercise on secondary lymphedema in breast cancer patients: a pilot study. J Clin Oncol. 2003;21(3):463–466. doi: 10.1200/JCO.2003.04.069.
    1. Mutrie N, Campbell AM, Whyte F, McConnachie A, Emslie C, Lee L, Kearney N, Walker A, Ritchie D. Benefits of supervised group exercise programme for women being treated for early stage breast cancer: pragmatic randomised controlled trial. BMJ. 2007;334(7592):517. doi: 10.1136/.
    1. Campbell A, Mutrie N, White F, McGuire F, Kearney N. A pilot study of a supervised group exercise programme as a rehabilitation treatment for women with breast cancer receiving adjuvant treatment. Eur J Oncol Nurs. 2005;9(1):56–63. doi: 10.1016/j.ejon.2004.03.007.
    1. Thomson CA, Thompson PA, Wright-Bea J, Nardi E, Frey GR, Stopeck A. Metabolic syndrome and elevated C-reactive protein in breast cancer survivors on adjuvant hormone therapy. J Womens Health (Larchmt) 2009;18(12):2041–2047. doi: 10.1089/jwh.2009.1365.
    1. de Haas EC, Oosting SF, Lefrandt JD, Wolffenbuttel BH, Sleijfer DT, Gietema JA. The metabolic syndrome in cancer survivors. Lancet Oncol. 2010;11(2):193–203. doi: 10.1016/S1470-2045(09)70287-6.
    1. Grundy SM. Metabolic syndrome pandemic. Arterioscler Thromb Vasc Biol. 2008;28(4):629–636. doi: 10.1161/ATVBAHA.107.151092.
    1. Metkus TS Jr, Baughman KL, Thompson PD. Exercise prescription and primary prevention of cardiovascular disease. Circulation. 2010;121(23):2601–2604. doi: 10.1161/CIRCULATIONAHA.109.903377.
    1. Bluher M, Zimmer P. [Metabolic and cardiovascular effects of physical activity, exercise and fitness in patients with type 2 diabetes] Dtsch Med Wochenschr. 2010;135(18):930–934. doi: 10.1055/s-0030-1253682.
    1. Healy LA, Ryan AM, Carroll P, Ennis D, Crowley V, Boyle T, Kennedy MJ, Connolly E, Reynolds JV. Metabolic syndrome, central obesity and insulin resistance are associated with adverse pathological features in postmenopausal breast cancer. Arterioscler Thromb Vasc Biol. 2010;22(4):281–288.
    1. Emaus A, Veierod MB, Tretli S, Finstad SE, Selmer R, Furberg AS, Bernstein L, Schlichting E, Thune I. Metabolic profile, physical activity, and mortality in breast cancer patients. Breast Cancer Res Treat. 2010;121(3):651–660. doi: 10.1007/s10549-009-0603-y.
    1. Demark-Wahnefried W, Peterson BL, Winer EP, Marks L, Aziz N, Marcom PK, Blackwell K, Rimer BK. Changes in weight, body composition, and factors influencing energy balance among premenopausal breast cancer patients receiving adjuvant chemotherapy. J Clin Oncol. 2001;19(9):2381–2389.
    1. Vehmanen L, Saarto T, Blomqvist C, Taskinen MR, Elomaa I. Tamoxifen treatment reverses the adverse effects of chemotherapy-induced ovarian failure on serum lipids. Br J Cancer. 2004;91(3):476–481. doi: 10.1038/sj.bjc.6601979.
    1. Grundy SM. Drug therapy of the metabolic syndrome: minimizing the emerging crisis in polypharmacy. Nat Rev Drug Discov. 2006;5(4):295–309. doi: 10.1038/nrd2005.
    1. Goodwin PJ, Ligibel JA, Stambolic V. Metformin in breast cancer: time for action. J Clin Oncol. 2009;27(20):3271–3273. doi: 10.1200/JCO.2009.22.1630.
    1. Krentz AJ, Patel MB, Bailey CJ. New drugs for type 2 diabetes mellitus: what is their place in therapy? Drugs. 2008;68(15):2131–2162. doi: 10.2165/00003495-200868150-00005.
    1. Fairey AS, Courneya KS, Field CJ, Bell GJ, Jones LW, Mackey JR. Effects of exercise training on fasting insulin, insulin resistance, insulin-like growth factors, and insulin-like growth factor binding proteins in postmenopausal breast cancer survivors: a randomized controlled trial. Cancer Epidemiol Biomarkers Prev. 2003;12(8):721–727.
    1. Ligibel JA, Campbell N, Partridge A, Chen WY, Salinardi T, Chen H, Adloff K, Keshaviah A, Winer EP. Impact of a mixed strength and endurance exercise intervention on insulin levels in breast cancer survivors. J Clin Oncol. 2008;26(6):907–912. doi: 10.1200/JCO.2007.12.7357.
    1. Hayes SC, Spence RR, Galvao DA, Newton RU. Australian association for exercise and sport science position stand: optimising cancer outcomes through exercise. J Sci Med Sport. 2009;12(4):428–434. doi: 10.1016/j.jsams.2009.03.002.
    1. Newton RU, Galvao DA. Exercise in prevention and management of cancer. Curr Treat Options Oncol. 2008;9(2–3):135–146.
    1. Schmitz KH, Courneya KS, Matthews C, Demark-Wahnefried W, Galvao DA, Pinto BM, Irwin ML, Wolin KY, Segal RJ, Lucia A, Schneider CM, von Gruenigen VE, Schwartz AL. American college of sports medicine roundtable on exercise guidelines for cancer survivors. Med Sci Sports Exerc. 2010;42(7):1409–1426.
    1. Neilson HK, Friedenreich CM, Brockton NT, Millikan RC. Physical activity and postmenopausal breast cancer: proposed biologic mechanisms and areas for future research. Cancer Epidemiol Biomarkers Prev. 2009;18(1):11–27. doi: 10.1158/1055-9965.EPI-08-0756.
    1. Sveklina TS, Talantseva MS, Barsukov A. [The metabolic syndrome and inflammation: actual issues of pathogenesis] Klin Lab Diagn. 2013;3:7–10.
    1. Ebbeling CB, Ward A, Puleo EM, Widrick J, Rippe JM. Development of a single-stage submaximal treadmill walking test. Med Sci Sports Exerc. 1991;23(8):966–973.
    1. Jones LW, Eves ND, Haykowsky M, Joy AA, Douglas PS. Cardiorespiratory exercise testing in clinical oncology research: systematic review and practice recommendations. Lancet Oncol. 2008;9(8):757–765. doi: 10.1016/S1470-2045(08)70195-5.
    1. Brzycki M. Strength testing: predicting a one-rep max from repetition-to-fatigue. JOHPERD. 1993;64:88–90.
    1. Prior BM, Cureton KJ, Modlesky CM, Evans EM, Sloniger MA, Saunders M, Lewis RD. In vivo validation of whole body composition estimates from dual-energy X-ray absorptiometry. J Appl Physiol. 1997;83(2):623–630.
    1. Valentinuzzi ME. Bioelectrical impedance techniques in medicine. Part I: Bioimpedance measurement. First section: general concepts. Crit Rev Biomed Eng. 1996;24(4–6):223–255.
    1. Harrington S, Padua D, Battaglini C, Michener LA. Upper extremity strength and range of motion and their relationship to function in breast cancer survivors. Physiother Theory Pract. 2013.
    1. Taylor R, Jayasinghe UW, Koelmeyer L, Ung O, Boyages J. Reliability and validity of arm volume measurements for assessment of lymphedema. Phys Ther. 2006;86(2):205–214.
    1. Kriska AM, Knowler WC, LaPorte RE, Drash AL, Wing RR, Blair SN, Bennett PH, Kuller LH. Development of questionnaire to examine relationship of physical activity and diabetes in Pima Indians. Diabetes Care. 1990;13(4):401–411. doi: 10.2337/diacare.13.4.401.
    1. Irwin ML, Tworoger SS, Yasui Y, Rajan B, McVarish L, LaCroix K, Ulrich CM, Bowen D, Schwartz RS, Potter JD, McTiernan A. Influence of demographic, physiologic, and psychosocial variables on adherence to a yearlong moderate-intensity exercise trial in postmenopausal women. Prev Med. 2004;39(6):1080–1086. doi: 10.1016/j.ypmed.2004.04.017.
    1. Neuhouser ML, Kristal AR, McLerran D, Patterson RE, Atkinson J. Validity of short food frequency questionnaires used in cancer chemoprevention trials: results from the prostate cancer prevention trial. Cancer Epidemiol Biomarkers Prev. 1999;8(8):721–725.
    1. Snyder DC, Morey MC, Sloane R, Stull V, Cohen HJ, Peterson B, Pieper C, Hartman TJ, Miller PE, Mitchell DC, Demark-Wahnefried W. Reach out to ENhancE wellness in older cancer survivors (RENEW): design, methods and recruitment challenges of a home-based exercise and diet intervention to improve physical function among long-term survivors of breast, prostate, and colorectal cancer. Psychooncology. 2009;18(4):429–439. doi: 10.1002/pon.1491.
    1. Brady MJ, Cella DF, Mo F, Bonomi AE, Tulsky DS, Lloyd SR, Deasy S, Cobleigh M, Shiomoto G. Reliability and validity of the functional assessment of cancer therapy-breast quality-of-life instrument. J Clin Oncol. 1997;15(3):974–986.
    1. Andresen EM, Malmgren JA, Carter WB, Patrick DL. Screening for depression in well older adults: evaluation of a short form of the CES-D (center for epidemiologic studies depression scale) Am J Prev Med. 1994;10(2):77–84.
    1. Harrington S, Padua D, Battaglini C, Michener LA, Giuliani C, Myers J, Groff D. Comparison of shoulder flexibility, strength, and function between breast cancer survivors and healthy participants. J Cancer Surviv. 2011;5(2):167–174. doi: 10.1007/s11764-010-0168-0.
    1. Leggin BG, Michener LA, Shaffer MA, Brenneman SK, Iannotti JP, Williams GR Jr. The Penn shoulder score: reliability and validity. J Orthop Sports Phys Ther. 2006;36(3):138–151. doi: 10.2519/jospt.2006.36.3.138.
    1. Denke MA, Pasternak RC. Defining and treating the metabolic syndrome: a primer from the adult treatment panel III. Curr Treat Options Cardiovasc Med. 2001;3(4):251–253. doi: 10.1007/s11936-001-0087-5.
    1. Nuver J, Smit AJ, Postma A, Sleijfer DT, Gietema JA. The metabolic syndrome in long-term cancer survivors, an important target for secondary preventive measures. Cancer Treat Rev. 2002;28(4):195–214. doi: 10.1016/S0305-7372(02)00038-5.
    1. Redig AJ, Munshi HG. Care of the cancer survivor: metabolic syndrome after hormone-modifying therapy. The American journal of medicine. 2010;123(1):87. e81-86.
    1. Cowey S, Hardy RW. The metabolic syndrome: a high-risk state for cancer? Am J Pathol. 2006;169(5):1505–1522. doi: 10.2353/ajpath.2006.051090.
    1. Dai DF, Hwang JJ, Chen CL, Chiang FT, Lin JL, Hsu KL, Tseng CD, Tseng YZ. Effect of physical activity on the prevalence of metabolic syndrome and left ventricular hypertrophy in apparently healthy adults. J Formos Med Assoc. 2010;109(10):716–724. doi: 10.1016/S0929-6646(10)60116-7.
    1. Nguyen TH, Tang HK, Kelly P, van der Ploeg HP, Dibley MJ. Association between physical activity and metabolic syndrome: a cross sectional survey in adolescents in Ho Chi Minh City, Vietnam. BMC Public Health. 2010;10:141. doi: 10.1186/1471-2458-10-141.
    1. Harralson TL, Uplinger N, McLaughlin M. Increasing physical activity: a step toward controlling metabolic syndrome. Diabetes Educ. 2010;36(1):70–71. doi: 10.1177/0145721709358461.
    1. van Waas M, Neggers SJ, van der Lelij AJ, Pieters R, van den Heuvel-Eibrink MM. The metabolic syndrome in adult survivors of childhood cancer, a review. J Pediatr Hematol Oncol. 2010;32(3):171–179. doi: 10.1097/MPH.0b013e3181d419c3.
    1. Bao PP, Zheng Y, Nechuta S, Gu K, Cai H, Peng P, Shu XO, Lu W. Exercise after diagnosis and metabolic syndrome among breast cancer survivors: a report from the shanghai breast cancer survival study. Cancer Causes Control. 2013;24(9):1747–1756. doi: 10.1007/s10552-013-0252-7.
    1. Leon AS, Sanchez OA. Response of blood lipids to exercise training alone or combined with dietary intervention. Medicine and science in sports and exercise. 2001;33(6 Suppl):S502–515. discussion S528-509.
    1. Byberg L, Zethelius B, McKeigue PM, Lithell HO. Changes in physical activity are associated with changes in metabolic cardiovascular risk factors. Diabetologia. 2001;44(12):2134–2139. doi: 10.1007/s001250100022.
    1. Moreau KL, Degarmo R, Langley J, McMahon C, Howley ET, Bassett DR Jr, Thompson DL. Increasing daily walking lowers blood pressure in postmenopausal women. Med Sci Sports Exerc. 2001;33(11):1825–1831.
    1. Irwin ML, Mayer-Davis EJ, Addy CL, Pate RR, Durstine JL, Stolarczyk LM, Ainsworth BE. Moderate-intensity physical activity and fasting insulin levels in women: the cross-cultural activity participation study. Diabetes Care. 2000;23(4):449–454. doi: 10.2337/diacare.23.4.449.
    1. Ibanez J, Izquierdo M, Martinez-Labari C, Ortega F, Grijalba A, Forga L, Idoate F, Garcia-Unciti M, Fernandez-Real JM, Gorostiaga EM. Resistance training improves cardiovascular risk factors in obese women despite a significative decrease in serum adiponectin levels. Obesity (Silver Spring) 2010;18(3):535–541. doi: 10.1038/oby.2009.277.
    1. Dipietro L, Yeckel CW, Dziura J. Progressive improvement in glucose tolerance following lower-intensity resistance versus moderate-intensity aerobic training in older women. J Phys Act Health. 2008;5(6):854–869.
    1. Fenicchia LM, Kanaley JA, Azevedo JL Jr, Miller CS, Weinstock RS, Carhart RL, Ploutz-Snyder LL. Influence of resistance exercise training on glucose control in women with type 2 diabetes. Metabolism. 2004;53(3):284–289. doi: 10.1016/j.metabol.2003.10.007.
    1. Rogers LQ, Markwell SJ, Verhulst S, McAuley E, Courneya KS. Rural breast cancer survivors: exercise preferences and their determinants. Psychooncology. 2009;18(4):412–421. doi: 10.1002/pon.1497.
    1. Milne HM, Guilfoyle A, Gordon S, Wallman KE, Courneya KS. Personal accounts of exercise and quality of life from the perspective of breast cancer survivors. Qual Life Res. 2007;16(9):1473–1481. doi: 10.1007/s11136-007-9251-z.
    1. State & County Quick Facts. State & County Quick Facts. [ ]
    1. Demark-Wahnefried W, Aziz NM, Rowland JH, Pinto BM. Riding the crest of the teachable moment: promoting long-term health after the diagnosis of cancer. J Clin Oncol. 2005;23(24):5814–5830. doi: 10.1200/JCO.2005.01.230.
    1. McBride CM, Clipp E, Peterson BL, Lipkus IM, Demark-Wahnefried W. Psychological impact of diagnosis and risk reduction among cancer survivors. Psychooncology. 2000;9(5):418–427. doi: 10.1002/1099-1611(200009/10)9:5<418::AID-PON474>;2-E.
    1. Spark LC, Reeves MM, Fjeldsoe BS, Eakin EG. Physical activity and/or dietary interventions in breast cancer survivors: a systematic review of the maintenance of outcomes. J Cancer Surviv. 2013;7(1):74–82. doi: 10.1007/s11764-012-0246-6.
    1. Latka RN, Alvarez-Reeves M, Cadmus L, Irwin ML. Adherence to a randomized controlled trial of aerobic exercise in breast cancer survivors: the Yale exercise and survivorship study. J Cancer Surviv. 2009;3(3):148–157. doi: 10.1007/s11764-009-0088-z.
    1. Irwin ML, Cadmus L, Alvarez-Reeves M, O’Neil M, Mierzejewski E, Latka R, Yu H, Dipietro L, Jones B, Knobf MT, Chung GG, Mayne ST. Recruiting and retaining breast cancer survivors into a randomized controlled exercise trial: the yale exercise and survivorship study. Cancer. 2008;112(11 Suppl):2593–2606.

Source: PubMed

3
Abonneren