Skip to main content

Advertisement

SpringerLink
Log in

Effects of an exercise and hypocaloric healthy eating program on biomarkers associated with long-term prognosis after early-stage breast cancer: a randomized controlled trial

  • Original paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Excess body weight at diagnosis and weight gain after breast cancer are associated with poorer long-term prognosis. This study investigated the effects of a lifestyle intervention on body weight and other health outcomes influencing long-term prognosis in overweight women (BMI > 25.0 kg/m2) recovering from early-stage (stage I–III) breast cancer. A total of 90 women treated 3–18 months previously were randomly allocated to a 6-month exercise and hypocaloric healthy eating program (n = 47, aged 55.6 ± 10.2 year) or control group (n = 43, aged 55.9 ± 8.9 year). Women in the intervention group received three supervised exercise sessions per week and individualized dietary advice, supplemented by weekly nutrition seminars. Body weight, waist circumference, waist/hip ratio [WHR], cardiorespiratory fitness, blood biomarkers associated with breast cancer recurrence and cardiovascular disease risk, and quality of life (FACT-B) were assessed at baseline and 6 months. Three-day diet diaries were used to assess macronutrient and energy intakes. A moderate reduction in body weight in the intervention group (median difference from baseline of −1.09 kg; IQR −0.15 to −2.90 kg; p = 0.07) was accompanied by significant reductions in waist circumference (p < 0.001), WHR (p = 0.005), total (p = 0.021) and saturated fat (p = 0.006) intakes, leptin (p = 0.005), total cholesterol (p = 0.046), and resting diastolic blood pressure (p = 0.03). Cardiopulmonary fitness (p < 0.001) and FACT-B quality of life (p = 0.004) also showed significant improvements in the intervention group. These findings suggest that an individualized exercise and a hypocaloric healthy eating program can positively impact upon health outcomes influencing long-term prognosis in overweight women recovering from early-stage breast cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Mosher CE, Sloane R, Morey MC, Snyder DC, Cohen HJ, Miller PE, Demark-Wahnefried W (2009) Associations between lifestyle factors and quality of life among older long-term breast, prostate, and colorectal cancer survivors. Cancer 115:4001–4009

    Article  PubMed  Google Scholar 

  2. Voskuil DW, van Nes JG, Junggeburt JM, van de Velde CJ, van Leeuwen FE, de Haes JC (2010) Maintenance of physical activity and body weight in relation to subsequent quality of life in postmenopausal breast cancer patients. Ann Oncol 21:2094–2101

    Article  PubMed  CAS  Google Scholar 

  3. Rock CL, Demark-Wahnefried W (2002) Nutrition and survival after the diagnosis of breast cancer: a review of the evidence. J Clin Oncol 20:3302–3316

    Article  PubMed  Google Scholar 

  4. Nichols HB, Trentham-Dietz A, Egan KM, Titus-Ernstoff L, Holmes MD, Bersch AJ, Holick CN, Hampton JM, Stampfer MJ, Willett WC, Newcomb PA (2009) Body mass index before and after breast cancer diagnosis: associations with all-cause, breast cancer, and cardiovascular disease mortality. Cancer Epidemiol Biomarkers Prev 18:1403–1409

    Article  PubMed  Google Scholar 

  5. Kroenke CH, Chen WY, Rosner B, Holmes MD (2005) Weight, weight gain, and survival after breast cancer diagnosis. J Clin Oncol 23:1370–1378

    Article  PubMed  Google Scholar 

  6. McTiernan A, Rajan KB, Tworoger SS, Irwin M, Bernstein L, Baumgartner R, Gilliland F, Stanczyk FZ, Yasui Y, Ballard-Barbash R (2003) Adiposity and sex hormones in postmenopausal breast cancer survivors. J Clin Oncol 21:1961–1966

    Article  PubMed  CAS  Google Scholar 

  7. Campbell KL, McTiernan A (2007) Exercise and biomarkers for cancer prevention studies. J Nutr 137:161S–169S

    PubMed  CAS  Google Scholar 

  8. Festa A, D’Agostino R Jr, Williams K, Karter AJ, Mayer-Davis EJ, Tracy RP, Haffner SM (2001) The relation of body fat mass and distribution to markers of chronic inflammation. Int J Obes Relat Metab Disord 25:1407–1415

    Article  PubMed  CAS  Google Scholar 

  9. Despres JP, Lemieux I (2006) Abdominal obesity and metabolic syndrome. Nature 444:881–887

    Article  PubMed  CAS  Google Scholar 

  10. Balkwill F, Coussens LM (2004) Cancer: an inflammatory link. Nature 431:405–406

    Article  PubMed  CAS  Google Scholar 

  11. Kelesidis I, Kelesidis T, Mantzoros CS (2006) Adiponectin and cancer: a systematic review. Br J Cancer 94:1221–1225

    Article  PubMed  CAS  Google Scholar 

  12. Patnaik JL, Byers T, Diguiseppi C, Dabelea D, Denberg TD (2011) Cardiovascular disease competes with breast cancer as the leading cause of death for older females diagnosed with breast cancer: a retrospective cohort study. Breast Cancer Res 13:R64

    Article  PubMed  Google Scholar 

  13. Djuric Z, DiLaura NM, Jenkins I, Darga L, Jen CK, Mood D, Bradley E, Hryniuk WM (2002) Combining weight-loss counseling with the weight watchers plan for obese breast cancer survivors. Obes Res 10:657–665

    Article  PubMed  Google Scholar 

  14. Jen KL, Djuric Z, DiLaura NM, Buison A, Redd JN, Maranci V, Hryniuk WM (2004) Improvement of metabolism among obese breast cancer survivors in differing weight loss regimens. Obes Res 12:306–312

    Article  PubMed  Google Scholar 

  15. Chlebowski RT, Blackburn GL, Thomson CA, Nixon DW, Shapiro A, Hoy MK, Goodman MT, Giuliano AE, Karanja N, McAndrew P, Hudis C, Butler J, Merkel D, Kristal A, Caan B, Michaelson R, Vinciguerra V, Del PS, Winkler M, Hall R, Simon M, Winters BL, Elashoff RM (2006) Dietary fat reduction and breast cancer outcome: interim efficacy results from the Women’s Intervention Nutrition Study. J Natl Cancer Inst 98:1767–1776

    Article  PubMed  Google Scholar 

  16. Donnelly JE, Blair SN, Jakicic JM, Manore MM, Rankin JW, Smith BK (2009) American College of Sports Medicine Position Stand. Appropriate physical activity intervention strategies for weight loss and prevention of weight regain for adults. Med Sci Sports Exerc 41:459–471

    PubMed  Google Scholar 

  17. Shaw K, Gennat H, O’Rourke P, Del MC (2006) Exercise for overweight or obesity. Cochrane Database Systematic Review 18(4):CD003817

    Google Scholar 

  18. Wu T, Gao X, Chen M, van Dam RM (2009) Long-term effectiveness of diet-plus-exercise interventions vs. diet-only interventions for weight loss: a meta-analysis. Obes Rev 10:313–323

    Article  PubMed  CAS  Google Scholar 

  19. Demark-Wahnefried W, Case LD, Blackwell K, Marcom PK, Kraus W, Aziz N, Snyder DC, Giguere JK, Shaw E (2008) Results of a diet/exercise feasibility trial to prevent adverse body composition change in breast cancer patients on adjuvant chemotherapy. Clin Breast Cancer 8:70–79

    Article  PubMed  Google Scholar 

  20. Holmes MD, Chen WY, Feskanich D, Kroenke CH, Colditz GA (2005) Physical activity and survival after breast cancer diagnosis. JAMA 293:2479–2486

    Article  PubMed  CAS  Google Scholar 

  21. Holick CN, Newcomb PA, Trentham-Dietz A, Titus-Ernstoff L, Bersch AJ, Stampfer MJ, Baron JA, Egan KM, Willett WC (2008) Physical activity and survival after diagnosis of invasive breast cancer. Cancer Epidemiol Biomarkers Prev 17:379–386

    Article  PubMed  Google Scholar 

  22. Irwin ML (2009) Physical activity interventions for cancer survivors. Br J Sports Med 43:32–38

    Article  PubMed  CAS  Google Scholar 

  23. Pierce JP, Stefanick ML, Flatt SW, Natarajan L, Sternfeld B, Madlensky L, Al-Delaimy WK, Thomson CA, Kealey S, Hajek R, Parker BA, Newman VA, Caan B, Rock CL (2007) Greater survival after breast cancer in physically active women with high vegetable-fruit intake regardless of obesity. J Clin Oncol 25:2345–2351

    Article  PubMed  Google Scholar 

  24. McNeely ML, Campbell KL, Rowe BH, Klassen TP, Mackey JR, Courneya KS (2006) Effects of exercise on breast cancer patients and survivors: a systematic review and meta-analysis. CMAJ 175:34–41

    Article  PubMed  Google Scholar 

  25. Schmitz KH, Courneya KS, Matthews C, Demark-Wahnefried W, Galvão DA, Pinto BM, Irwin ML, Wolin KY, Segal RJ, Lucia A, Schneider CM, von Gruenigen VE, Schwartz AL (2010) American College of Sports Medicine roundtable on exercise guidelines for cancer survivors. Med Sci Sports Exerc 42:1409–1426

    Article  PubMed  Google Scholar 

  26. Utter AC, Nieman DC, Shannonhouse EM, Butterworth DE, Nieman CN (1998) Influence of diet and/or exercise on body composition and cardiorespiratory fitness in obese women. Int J Sports Nutr 8:213–222

    CAS  Google Scholar 

  27. Kaukua J, Pekkarinen T, Mustajoki P (2003) Health-related quality of life in obese outpatients losing weight with very-low-energy diet and behavioural modification: a 2 year follow-up study. Int J Obes Relat Metab Disord 27:1233–1241

    Article  PubMed  CAS  Google Scholar 

  28. Wadden TA, Steen SN, Wingate BJ, Foster GD (1996) Psychosocial consequences of weight reduction: how much weight loss is enough? Am J Clin Nutr 63:461S–465S

    PubMed  CAS  Google Scholar 

  29. Ebbeling CB, Ward A, Puleo EM, Widrick J, Rippe JM (1991) Development of a single-stage submaximal treadmill walking test. Med Sci Sports Exerc 23:966–973

    PubMed  CAS  Google Scholar 

  30. Cella DF, Tulsky DS, Gray G, Serafin B, Linn E, Bonomi A, Silberman M, Yellen SB, Wincour P, Brannon J (1993) The functional assessment of cancer therapy scale: development and validation of the general measure. J Clin Oncol 11:570–579

    PubMed  CAS  Google Scholar 

  31. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419

    Article  PubMed  CAS  Google Scholar 

  32. Demark-Wahnefried W, Clipp EC, Lipkus IM, Lobach D, Snyder DC, Sloane R, Peterson B, Macri JM, Rock CL, McBride CM, Kraus WE (2007) Main outcomes of the FRESH START trial: a sequentially tailored, diet and exercise mailed print intervention among breast and prostate cancer survivors. J Clin Oncol 25:2709–2718

    Article  PubMed  Google Scholar 

  33. Demark-Wahnefried W, Kenyon AJ, Eberle P, Skye A, Kraus WE (2002) Preventing sarcopenic obesity among breast cancer patients who receive adjuvant chemotherapy: results of a feasibility study. Clin Exerc Physiol 4:44–49

    PubMed  Google Scholar 

  34. McTiernan A, Ulrich C, Kumai C, Bean D, Schwartz R, Mahloch J, Hastings R, Gralow J, Potter JD (1998) Anthropometric and hormone effects of an eight-week exercise-diet intervention in breast cancer patients: results of a pilot study. Cancer Epidemiol Biomarkers Prev 7:477–481

    PubMed  CAS  Google Scholar 

  35. Morey MC, Snyder DC, Sloane R, Cohen HJ, Peterson B, Hartman TJ, Miller P, Mitchell DC, Demark-Wahnefried W (2009) Effects of home-based diet and exercise on functional outcomes among older, overweight long-term cancer survivors: RENEW: a randomized controlled trial. JAMA 301:1883–1891

    Article  PubMed  CAS  Google Scholar 

  36. Goodwin P, Esplen MJ, Butler K, Winocur J, Pritchard K, Brazel S, Gao J, Miller A (1998) Multidisciplinary weight management in locoregional breast cancer: results of a phase II study. Breast Cancer Res Treat 48:53–64

    Article  PubMed  CAS  Google Scholar 

  37. Powell LA, Nieman DC, Melby C, Cureton K, Schmidt D, Howley ET, Hill JO, Mault JR, Alexander H, Stewart DJ (2001) Assessment of body composition change in a community-based weight management program. J Am Coll Nutr 20:26–31

    PubMed  CAS  Google Scholar 

  38. Pakiz B, Flatt SW, Bardwell WA, Rock CL, Mills PJ (2011) Effects of a weight loss intervention on body mass, fitness, and inflammatory biomarkers in overweight or obese breast cancer survivors. Int J Behav Med 18:333–341

    Article  PubMed  Google Scholar 

  39. Vance V, Mourtzakis M, McCargar L, Hanning R (2011) Weight gain in breast cancer survivors: prevalence, pattern and health consequences. Obes Rev 12:282–294

    Article  PubMed  CAS  Google Scholar 

  40. Harvie M (2010) The importance of controlling body weight after a diagnosis of breast cancer: the role of diet and exercise in breast cancer patient management. In: Saxton JM, Daley AJ (eds) Exercise and cancer survivorship: impact on health outcomes and quality of life. Springer, New York, pp 73–96

    Chapter  Google Scholar 

  41. Irwin ML (2010) The biological mechanisms by which physical activity might have an impact on outcome/prognosis after a breast cancer diagnosis. In: Saxton JM, Daley AJ (eds) Exercise and cancer survivorship: impact on health outcomes and quality of life. Springer, New York, pp 97–112

    Chapter  Google Scholar 

  42. Goodwin PJ, Ennis M, Pritchard KI, Trudeau ME, Koo J, Taylor SK, Hood N (2012) Insulin- and obesity-related variables in early-stage breast cancer: correlations and time course of prognostic associations. J Clin Oncol 30:164–171

    Article  PubMed  Google Scholar 

  43. Martini G, Valenti R, Giovani S, Campagna S, Franci B, Nuti R (2001) Leptin and body composition in healthy postmenopausal women. Panminerva Med 43:149–154

    PubMed  CAS  Google Scholar 

  44. Gami AS, Witt BJ, Howard DE, Erwin PJ, Gami LA, Somers VK, Montori VM (2007) Metabolic syndrome and risk of incident cardiovascular events and death: a systematic review and meta-analysis of longitudinal studies. J Am Coll Cardiol 49:403–414

    Article  PubMed  CAS  Google Scholar 

  45. Rosato V, Bosetti C, Talamini R, Levi F, Montella M, Giacosa A, Negri E, La Vecchia C (2011) Metabolic syndrome and the risk of breast cancer in postmenopausal women. Ann Oncol 22:2687–2692

    Article  PubMed  CAS  Google Scholar 

  46. Bjorge T, Lukanova A, Jonsson H, Tretli S, Ulmer H, Manjer J, Stocks T, Selmer R, Nagel G, Almquist M, Concin H, Hallmans G, Haggstrom C, Stattin P, Engeland A (2010) Metabolic syndrome and breast cancer in the me-can (metabolic syndrome and cancer) project. Cancer Epidemiol Biomarkers Prev 19:1737–1745

    Article  PubMed  Google Scholar 

  47. Pierce BL, Ballard-Barbash R, Bernstein L, Baumgartner RN, Neuhouser ML, Wener MH, Baumgartner KB, Gilliland FD, Sorensen BE, McTiernan A, Ulrich CM (2009) Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. J Clin Oncol 27:3437–3444

    Article  PubMed  CAS  Google Scholar 

  48. Thomson CA, Thompson PA, Wright-Bea J, Nardi E, Frey GR, Stopeck A (2009) Metabolic syndrome and elevated C-reactive protein in breast cancer survivors on adjuvant hormone therapy. J Womens Health (Larchmt) 18:2041–2047

    Article  Google Scholar 

  49. Havel PJ, Kasim-Karakas S, Mueller W, Johnson PR, Gingerich RL, Stern JS (1996) Relationship of plasma leptin to plasma insulin and adiposity in normal weight and overweight women: effects of dietary fat content and sustained weight loss. J Clin Endocrinol Metab 81:4406–4413

    Article  PubMed  CAS  Google Scholar 

  50. Christensen JO, Svendsen OL, Hassager C, Christiansen C (1998) Leptin in overweight postmenopausal women: no relationship with metabolic syndrome X or effect of exercise in addition to diet. Int J Obes Relat Metab Disord 22:195–199

    Article  PubMed  CAS  Google Scholar 

  51. Bellizzi KM, Rowland JH, Jeffery DD, McNeel T (2005) Health behaviors of cancer survivors: examining opportunities for cancer control intervention. J Clin Oncol 23:8884–8893

    Article  PubMed  Google Scholar 

  52. Eton DT, Cella D, Yost KJ, Yount SE, Peterman AH, Neuberg DS, Sledge GW, Wood WC (2004) A combination of distribution- and anchor-based approaches determined minimally important differences (MIDs) for four endpoints in a breast cancer scale. J Clin Epidemiol 57:898–910

    Article  PubMed  Google Scholar 

  53. Bardwell WA, Major JM, Rock CL, Newman VA, Thomson CA, Chilton JA, Dimsdale JE, Pierce JP (2004) Health-related quality of life in women previously treated for early-stage breast cancer. Psychooncology 13:595–604

    Article  PubMed  Google Scholar 

  54. Darga LL, Magnan M, Mood D, Hryniuk WM, DiLaura NM, Djuric Z (2007) Quality of life as a predictor of weight loss in obese, early-stage breast cancer survivors. Oncol Nurs Forum 34:86–92

    Article  PubMed  Google Scholar 

  55. Daley AJ, Crank H, Saxton JM, Mutrie N, Coleman R, Roalfe A (2007) Randomized trial of exercise therapy in women treated for breast cancer. J Clin Oncol 25:1713–1721

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a Project Grant from the American Institute for Cancer Research [Grant number 05A008-REV].

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. School of Health and Related Research, University of Sheffield, Sheffield, UK

    E. Scott

  2. Department of Primary Care Clinical Sciences, University of Birmingham, Birmingham, UK

    A. J. Daley

  3. School of Medicine, Health Policy and Practice, University of East Anglia, Norwich, UK

    H. Doll

  4. Biomedical Research Centre, Sheffield Hallam University, Sheffield, UK

    N. Woodroofe

  5. CR-UK/YCR Sheffield Cancer Research Centre, Weston Park Hospital, University of Sheffield, Sheffield, UK

    R. E. Coleman

  6. Institute for Sport, Physical Education and Health Sciences, University of Edinburgh, Edinburgh, UK

    N. Mutrie

  7. Centre for Sport and Exercise Science, Sheffield Hallam University, Sheffield, UK

    H. Crank

  8. Human Nutrition Unit, Department of Oncology, University of Sheffield, Sheffield, UK

    H. J. Powers

  9. Faculty of Medicine and Health Sciences, School of Allied Health Professions, University of East Anglia, Room 2-8 Queen’s Building, Norwich, NR4 7TJ, UK

    J. M. Saxton

Authors
  1. E. Scott
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. J. Daley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H. Doll
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. N. Woodroofe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. E. Coleman
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. N. Mutrie
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. H. Crank
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. H. J. Powers
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. J. M. Saxton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. M. Saxton.

Additional information

International Standard Randomized Controlled Trial Number: ISRCTN08045231 http://www.controlled-trials.com/

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scott, E., Daley, A.J., Doll, H. et al. Effects of an exercise and hypocaloric healthy eating program on biomarkers associated with long-term prognosis after early-stage breast cancer: a randomized controlled trial. Cancer Causes Control 24, 181–191 (2013). https://doi.org/10.1007/s10552-012-0104-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-012-0104-x

Keywords

Search

Navigation