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Clinical Research

Dose-response effects of aerobic exercise on adiposity markers in postmenopausal women: pooled analyses from two randomized controlled trials

International Journal of Obesity volume 45, pages 1298–1309 (2021)Cite this article

Subjects

Abstract

Background/objective

Exercise may reduce the risk of breast cancer through adiposity changes, but the dose-response effects of exercise volume on adiposity markers are unknown in postmenopausal women. We aimed to compare the dose-response effects of prescribed aerobic exercise volume on adiposity outcomes.

Participants/methods

Data from the Alberta Physical Activity and Breast Cancer Prevention (ALPHA) and Breast Cancer and Exercise Trial in Alberta (BETA) were pooled for this analysis (N = 720). These were 12-month randomized controlled trials, where participants were randomized to 225 min/week (mid-volume) of aerobic exercise versus usual inactive lifestyle (ALPHA), or 150 min/week (low-volume) versus 300 min/week (high-volume) (BETA). Fat mass and fat-free mass were measured using DXA and intra-abdominal and subcutaneous fat area were assessed with computed tomography.

Results

After 12 months of aerobic exercise, increasing exercise volumes from no exercise/control to 300 min/week resulted in statistically significant reductions in BMI, weight, fat mass, fat percentage, intra-abdominal and subcutaneous fat area (P < 0.001). Compared with controls, fat mass loss was −1.13, −1.98 and −2.09 kg in the low-, mid- and high-volume groups, respectively. Similarly, weight loss was −1.47, −1.83, −2.21 kg in the low-, mid- and high-volume groups, respectively, compared to controls, and intra-abdominal fat area loss was −7.44, −15.56 and −8.76 cm2 in the low-, mid- and high-volume groups, respectively, compared to controls. No evidence for a dose-response effect on fat-free mass was noted.

Conclusion

A dose-response effect of exercise volume on adiposity markers was noted, however, the differences in adiposity markers were smaller when comparing 225 min/week to 300 min/week of exercise. Given the strong positive associations between obesity and postmenopausal breast cancer risk, this study provides evidence on the importance of exercise volume as part of the exercise prescription to reduce adiposity and, ultimately, postmenopausal breast cancer risk.

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Fig. 1: Participant flow diafram for the ALPHA Trial and BETA, Alberta, Canada, 2008–2012.

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References

  1. Lambrinoudaki I, Brincat M, Erel CT, Gambacciani M, Moen MH, Schenck-Gustafsson K, et al. EMAS position statement: managing obese postmenopausal women. Maturitas. 2010;66:323–6.

    Article  PubMed  Google Scholar 

  2. Greendale GA, Sternfeld B, Huang M, Han W, Karvonen-Gutierrez C, Ruppert K, et al. Changes in body composition and weight during the menopause transition. JCI Insight. 2019;4:e124865.

    Article  PubMed Central  Google Scholar 

  3. El Khoudary SR, Greendale G, Crawford SL, Avis NE, Brooks MM, Thurston RC, et al. The menopause transition and women’s health at midlife: a progress report from the Study of Women’s Health Across the Nation (SWAN). Menopause. 2019;26:1213–27.

    PubMed  PubMed Central  Google Scholar 

  4. Lovejoy JC, Champagne CM, de Jonge L, Xie H, Smith SR. Increased visceral fat and decreased energy expenditure during the menopausal transition. Int J Obes (Lond). 2008;32:949–58.

    Article  CAS  Google Scholar 

  5. Dennis KE. Postmenopausal women and the health consequences of obesity. J Obstet Gynecol Neonatal Nurs. 2007;36:511–7. quiz 518–9.

    Article  PubMed  Google Scholar 

  6. Arnold M, Pandeya N, Byrnes G, Renehan PAG, Stevens GA, Ezzati PM, et al. Global burden of cancer attributable to high body-mass index in 2012: a population-based study. Lancet Oncol. 2015;16:36–46.

    Article  PubMed  Google Scholar 

  7. Neuhouser ML, Aragaki AK, Prentice RL, Manson JE, Chlebowski R, Carty CL, et al. Overweight, Obesity, and Postmenopausal Invasive Breast Cancer Risk: A Secondary Analysis of the Women’s Health Initiative Randomized Clinical Trials. JAMA Oncol. 2015;1:611–21.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Picon-Ruiz M, Morata-Tarifa C, Valle-Goffin JJ, Friedman ER, Slingerland JM. Obesity and adverse breast cancer risk and outcome: Mechanistic insights and strategies for intervention. CA Cancer J Clin. 2017;67:378–97.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Neilson HK, Conroy SM, Friedenreich CM. The Influence of Energetic Factors on Biomarkers of Postmenopausal Breast Cancer Risk. Curr Nutr Rep. 2014;3:22–34.

    Article  CAS  PubMed  Google Scholar 

  10. Ligibel JA, Basen-Engquist K, Bea JW. Weight Management and Physical Activity for Breast Cancer Prevention and Control. Am Soc Clin Oncol Educ Book. 2019;39:e22–33.

    Article  PubMed  Google Scholar 

  11. Teede HJ, Lombard C, Deeks AA. Obesity, metabolic complications and the menopause: an opportunity for prevention. Climacteric. 2010;13:203–9.

    Article  CAS  PubMed  Google Scholar 

  12. Campbell KL, Foster-Schubert KE, Alfano CM, Wang CC, Wang CY, Duggan CR, et al. Reduced-calorie dietary weight loss, exercise, and sex hormones in postmenopausal women: randomized controlled trial. J Clin Oncol. 2012;30:2314–26.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Chlebowski RT, Luo J, Anderson GL, Barrington W, Reding K, Simon MS, et al. Weight loss and breast cancer incidence in postmenopausal women. Cancer. 2019;125:205–12.

    Article  PubMed  Google Scholar 

  14. Church TS, Earnest CP, Skinner JS, Blair SN. Effects of different doses of physical activity on cardiorespiratory fitness among sedentary, overweight or obese postmenopausal women with elevated blood pressure: a randomized controlled trial. JAMA. 2007;297:2081–91.

    Article  CAS  PubMed  Google Scholar 

  15. Bueno-Notivol J, Calvo-Latorre J, Alonso-Ventura V, Pasupuleti V, Hernandez AV, Perez-Lopez FR, et al. Effect of programmed exercise on insulin sensitivity in postmenopausal women: a systematic review and meta-analysis of randomized controlled trials. Menopause. 2017;24:1404–13.

    Article  PubMed  Google Scholar 

  16. Gonzalo-Encabo P, McNeil J, Boyne DJ, Courneya KS, Friedenreich CM. Dose-response effects of exercise on bone mineral density and content in post-menopausal women. Scand J Med Sci Sports. 2019;29:1121–9.

    Article  PubMed  Google Scholar 

  17. Gonzalo-Encabo P, Valades D, Garcia-Honduvilla N, de Cos Blanco A, Friedenreich CM, Perez-Lopez A. Exercise type and fat mass loss regulate breast cancer-related sex hormones in obese and overweight postmenopausal women. Eur J Appl Physiol. 2020;120:1277–87.

    Article  CAS  PubMed  Google Scholar 

  18. Donnelly JE, Blair SN, Jakicic JM, Manore MM, Rankin JW, Smith BK, et al. 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. 2009;41:459–71.

    Article  PubMed  Google Scholar 

  19. Bull FC, Al-Ansari SS, Biddle S, Borodulin K, Buman MP, Cardon G, et al. World Health Organization 2020 guidelines on physical activity and sedentary behaviour. Br J Sports Med. 2020;54:1451–62.

    Article  PubMed  Google Scholar 

  20. Piercy KL, Troiano RP, Ballard RM, Carlson SA, Fulton JE, Galuska DA, et al. The Physical Activity Guidelines for Americans. JAMA. 2018;320:2020–8.

    Article  PubMed  Google Scholar 

  21. Chen X, Wang Q, Zhang Y, Xie Q, Tan X. Physical Activity and Risk of Breast Cancer: a Meta-Analysis of 38 Cohort Studies in 45 Study Reports. Value Health. 2019;22:104–28.

    Article  PubMed  Google Scholar 

  22. Chan DSM, Abar L, Cariolou M, Nanu N, Greenwood DC, Bandera EV, et al. World Cancer Research Fund International: continuous Update Project-systematic literature review and meta-analysis of observational cohort studies on physical activity, sedentary behavior, adiposity, and weight change and breast cancer risk. Cancer Causes Control. 2019;30:1183–200.

    Article  PubMed  Google Scholar 

  23. Friedenreich CM, MacLaughlin S, Neilson HK, Stanczyk FZ, Yasui Y, Duha A, et al. Study design and methods for the Breast Cancer and Exercise Trial in Alberta (BETA). BMC Cancer. 2014;14:919.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Friedenreich CM, Woolcott CG, McTiernan A, Terry T, Brant R, Ballard-Barbash R, et al. Adiposity changes after a 1-year aerobic exercise intervention among postmenopausal women: a randomized controlled trial. Int J Obes (Lond). 2011;35:427–35.

    Article  CAS  Google Scholar 

  25. Friedenreich CM, Neilson HK, O’Reilly R, Duha A, Yasui Y, Morielli AR, et al. Effects of a High vs Moderate Volume of Aerobic Exercise on Adiposity Outcomes in Postmenopausal Women: a Randomized Clinical Trial. JAMA Oncol. 2015;1:766–76.

    Article  PubMed  Google Scholar 

  26. Friedenreich CM, Woolcott CG, McTiernan A, Ballard-Barbash R, Brant RF, Stanczyk FZ, et al. Alberta physical activity and breast cancer prevention trial: sex hormone changes in a year-long exercise intervention among postmenopausal women. J Clin Oncol. 2010;28:1458–66.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Friedenreich CM, Courneya KS, Neilson HK, Matthews CE, Willis G, Irwin M, et al. Reliability and validity of the Past Year Total Physical Activity Questionnaire. Am J Epidemiol. 2006;163:959–70.

    Article  PubMed  Google Scholar 

  28. Medicine ACoS. ACSM’s Guidelines for Exercise Testing and Prescription. 6th edn. Philadelphia: Lippincott Williams and Wilkins; 2000.

  29. Kohler A, King R, Bahls M, Gross S, Steveling A, Gartner S, et al. Cardiopulmonary fitness is strongly associated with body cell mass and fat-free mass: the Study of Health in Pomerania (SHIP). Scand J Med Sci Sports. 2018;28:1628–35.

    Article  CAS  PubMed  Google Scholar 

  30. Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, et al. American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc. 2011;43:1334–59.

    Article  PubMed  Google Scholar 

  31. Weinheimer EM, Sands LP, Campbell WW. A systematic review of the separate and combined effects of energy restriction and exercise on fat-free mass in middle-aged and older adults: implications for sarcopenic obesity. Nutr Rev. 2010;68:375–88.

    Article  PubMed  Google Scholar 

  32. Irwin ML, Yasui Y, Ulrich CM, Bowen D, Rudolph RE, Schwartz RS, et al. Effect of exercise on total and intra-abdominal body fat in postmenopausal women: a randomized controlled trial. JAMA. 2003;289:323–30.

    Article  PubMed  Google Scholar 

  33. Asikainen TM, Miilunpalo S, Kukkonen-Harjula K, Nenonen A, Pasanen M, Rinne M, et al. Walking trials in postmenopausal women: effect of low doses of exercise and exercise fractionization on coronary risk factors. Scand J Med Sci Sports. 2003;13:284–92.

    Article  PubMed  Google Scholar 

  34. Dalleck LC, Allen BA, Hanson BA, Borresen EC, Erickson ME, De Lap SL. Dose-response relationship between moderate-intensity exercise duration and coronary heart disease risk factors in postmenopausal women. J Womens Health (Larchmt). 2009;18:105–13.

    Article  Google Scholar 

  35. Pahk K, Joung C, Kim S. Visceral fat metabolic activity evaluated by preoperative (18)F-FDG PET/CT significantly affects axillary lymph node metastasis in postmenopausal luminal breast cancer. Sci Rep. 2020;10:1348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Donohoe CL, Doyle SL, Reynolds JV. Visceral adiposity, insulin resistance and cancer risk. Diabetol Metab Syndr. 2011;3:12.

    Article  PubMed  PubMed Central  Google Scholar 

  37. Merlotti C, Ceriani V, Morabito A, Pontiroli AE. Subcutaneous fat loss is greater than visceral fat loss with diet and exercise, weight-loss promoting drugs and bariatric surgery: a critical review and meta-analysis. Int J Obes (Lond). 2017;41:672–82.

    Article  CAS  Google Scholar 

  38. van Gemert WA, Peeters PH, May AM, Doornbos AJH, Elias SG, van der Palen J, et al. Effect of diet with or without exercise on abdominal fat in postmenopausal women - a randomised trial. BMC Public Health. 2019;19:174.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Nicklas BJ, Wang X, You T, Lyles MF, Demons J, Easter L, et al. Effect of exercise intensity on abdominal fat loss during calorie restriction in overweight and obese postmenopausal women: a randomized, controlled trial. Am J Clin Nutr. 2009;89:1043–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Chubak J, Ulrich CM, Tworoger SS, Sorensen B, Yasui Y, Irwin ML, et al. Effect of exercise on bone mineral density and lean mass in postmenopausal women. Med Sci Sports Exerc. 2006;38:1236–44.

    Article  PubMed  Google Scholar 

  41. Marin-Cascales E, Alcaraz PE, Ramos-Campo DJ, Rubio-Arias JA. Effects of multicomponent training on lean and bone mass in postmenopausal and older women: a systematic review. Menopause. 2018;25:346–56.

    Article  PubMed  Google Scholar 

  42. Konopka AR, Harber MP. Skeletal muscle hypertrophy after aerobic exercise training. Exerc Sport Sci Rev. 2014;42:53–61.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Martin-Rincon M, Perez-Lopez A, Morales-Alamo D, Perez-Suarez I, de Pablos-Velasco P, Perez-Valera M, et al. Exercise Mitigates the Loss of Muscle Mass by Attenuating the Activation of Autophagy during Severe Energy Deficit. Nutrients. 2019;11:2824.

    Article  CAS  PubMed Central  Google Scholar 

  44. Kusminski CM, Bickel PE, Scherer PE. Targeting adipose tissue in the treatment of obesity-associated diabetes. Nat Rev Drug Discov. 2016;15:639–60.

    Article  CAS  PubMed  Google Scholar 

  45. Crespi E, Bottai G, Santarpia L. Role of inflammation in obesity-related breast cancer. Curr Opin Pharmacol. 2016;31:114–22.

    Article  CAS  PubMed  Google Scholar 

  46. Trentham-Dietz A, Newcomb PA, Egan KM, Titus-Ernstoff L, Baron JA, Storer BE, et al. Weight change and risk of postmenopausal breast cancer (United States). Cancer Causes Control. 2000;11:533–42.

    Article  CAS  PubMed  Google Scholar 

  47. Pérez-López A, Gonzalo-Encabo P. Myokines relevance in exercise adaptations. A world still to be discovered. Arch Med Deporte. 2018;35:214–6.

    Google Scholar 

  48. Dethlefsen C, Pedersen KS, Hojman P. Every exercise bout matters: linking systemic exercise responses to breast cancer control. Breast Cancer Res Treat. 2017;162:399–408.

    Article  PubMed  Google Scholar 

  49. Dethlefsen C, Lillelund C, Midtgaard J, Andersen C, Pedersen BK, Christensen JF, et al. Exercise regulates breast cancer cell viability: systemic training adaptations versus acute exercise responses. Breast Cancer Res Treat. 2016;159:469–79.

    Article  PubMed  Google Scholar 

  50. Cava E, Yeat NC, Mittendorfer B. Preserving Healthy Muscle during Weight Loss. Adv Nutr. 2017;8:511–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Visser M, Pahor M, Taaffe DR, Goodpaster BH, Simonsick EM, Newman AB, et al. Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci. 2002;57:M326–32.

    Article  PubMed  Google Scholar 

  52. Goodpaster BH, Chomentowski P, Ward BK, Rossi A, Glynn NW, Delmonico MJ, et al. Effects of physical activity on strength and skeletal muscle fat infiltration in older adults: a randomized controlled trial. J Appl Physiol (1985). 2008;105:1498–503.

    Article  Google Scholar 

  53. Wu H, Ballantyne CM. Skeletal muscle inflammation and insulin resistance in obesity. J Clin Investig. 2017;127:43–54.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Maltais ML, Desroches J, Dionne IJ. Changes in muscle mass and strength after menopause. J Musculoskelet Neuronal Interact. 2009;9:186–97.

    CAS  PubMed  Google Scholar 

  55. McTiernan A, Sorensen B, Irwin ML, Morgan A, Yasui Y, Rudolph RE, et al. Exercise effect on weight and body fat in men and women. Obesity (Silver Spring). 2007;15:1496–512.

    Article  Google Scholar 

  56. van Gemert WA, Schuit AJ, van der Palen J, May AM, Iestra JA, Wittink H, et al. Effect of weight loss, with or without exercise, on body composition and sex hormones in postmenopausal women: the SHAPE-2 trial. Breast Cancer Res. 2015;17:120.

    Article  PubMed  PubMed Central  Google Scholar 

  57. McTiernan A. Behavioral risk factors in breast cancer: can risk be modified? Oncologist. 2003;8:326–34.

    Article  PubMed  Google Scholar 

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Acknowledgements

The ALPHA Trial was funded by a research grant (no. 017468) from the Canadian Breast Cancer Research Alliance. BETA was funded by a research grant from the Alberta Cancer Foundation (#24404). Paola Gonzalo-Encabo is supported by a Predoctoral Fellowship by the Spanish Ministry of Education, Culture and Sports. Dr JM is supported by a Postdoctoral Fellowship Awards from the Canadian Institutes of Health Research and Alberta Innovates-Health Solutions. Dr Kerry Courneya holds a Tier I Canada Research Chair. Dr Christine Friedenreich holds a Health Senior Scholar Award from Alberta Innovates-Health Solutions and the Alberta Cancer Foundation Weekend to End Women’s Cancers Breast Cancer Chair.

Funding

Research Grant No. 017468 from the Canadian Breast Cancer Research Alliance (ALPHA Trial); Research Grant No. 24404 from the Alberta Cancer Foundation (BETA Trial).

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Authors and Affiliations

  1. Department of Cancer Epidemiology and Prevention Research, Cancer Care Alberta, Alberta Health Services, Calgary, AB, Canada

    Paola Gonzalo-Encabo, Jessica McNeil & Christine M. Friedenreich

  2. Department of Biomedical Sciences, Area of Sport and Physical Education (GRIGEDE), University of Alcalá, Alcalá de Henares, Madrid, Spain

    Paola Gonzalo-Encabo, Alberto Pérez-López & David Valadés

  3. Department of Medicine and Medical Specialties, Faculty of Medicine and Health Sciences, University of Alcalá, Alcalá de Henares, Madrid, Spain

    Paola Gonzalo-Encabo

  4. Department of Kinesiology, School of Health and Human Sciences, University of North Carolina Greensboro, Greensboro, NC, USA

    Jessica McNeil

  5. Faculty of Kinesiology, Sport and Recreation, University of Alberta, Edmonton, AB, Canada

    Kerry S. Courneya

  6. Department of Community Health Sciences, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada

    Christine M. Friedenreich

  7. Department of Oncology, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada

    Christine M. Friedenreich

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  1. Paola Gonzalo-Encabo
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Correspondence to Christine M. Friedenreich.

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Gonzalo-Encabo, P., McNeil, J., Pérez-López, A. et al. Dose-response effects of aerobic exercise on adiposity markers in postmenopausal women: pooled analyses from two randomized controlled trials. Int J Obes 45, 1298–1309 (2021). https://doi.org/10.1038/s41366-021-00799-1

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