Effect of aerobic exercise intervention on markers of insulin resistance in breast cancer women
Corresponding Author
E. Bruno MSc
Research Fellow
Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Correspondence
Eleonora Bruno
Epidemiology & Prevention Unit, Department of Predictive & Preventive Medicine
Fondazione IRCCS Istituto Nazionale dei Tumori
Milano, Italy.
Email: [email protected]
Search for more papers by this authorE. Roveda MD
Assistant Professor
Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
Search for more papers by this authorJ. Vitale PhD
Research Fellow
IRCCS Istituto Ortopedico Galeazzi, Milan, Italy
Search for more papers by this authorA. Montaruli PhD
Assistant Professor
Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
Search for more papers by this authorF. Berrino MD
Former Head
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Search for more papers by this authorA. Villarini PhD
Senior Researcher
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Search for more papers by this authorE. Venturelli MSc
Senior Researcher
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Search for more papers by this authorG. Gargano PhD
Research Fellow
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Search for more papers by this authorL. Galasso MSc
Research Fellow
Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
Search for more papers by this authorA. Caumo PhD
Professor
Research Centre of Metabolism, IRCCS Policlinico San Donato Milanese, Milan, Italy
Search for more papers by this authorF. Carandente MD
Full Professor
Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
Search for more papers by this authorP. Pasanisi MD
Senior Researcher
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Search for more papers by this authorCorresponding Author
E. Bruno MSc
Research Fellow
Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Correspondence
Eleonora Bruno
Epidemiology & Prevention Unit, Department of Predictive & Preventive Medicine
Fondazione IRCCS Istituto Nazionale dei Tumori
Milano, Italy.
Email: [email protected]
Search for more papers by this authorE. Roveda MD
Assistant Professor
Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
Search for more papers by this authorJ. Vitale PhD
Research Fellow
IRCCS Istituto Ortopedico Galeazzi, Milan, Italy
Search for more papers by this authorA. Montaruli PhD
Assistant Professor
Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
Search for more papers by this authorF. Berrino MD
Former Head
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Search for more papers by this authorA. Villarini PhD
Senior Researcher
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Search for more papers by this authorE. Venturelli MSc
Senior Researcher
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Search for more papers by this authorG. Gargano PhD
Research Fellow
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Search for more papers by this authorL. Galasso MSc
Research Fellow
Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
Search for more papers by this authorA. Caumo PhD
Professor
Research Centre of Metabolism, IRCCS Policlinico San Donato Milanese, Milan, Italy
Search for more papers by this authorF. Carandente MD
Full Professor
Department of Biomedical Sciences for Health, University of Milan, Milan, Italy
Search for more papers by this authorP. Pasanisi MD
Senior Researcher
Department of Predictive & Preventive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan, Italy
Search for more papers by this authorAbstract
Insulin may affect breast cancer (BC) risk and prognosis. Exercise reduces insulin in obese BC survivors. We designed a randomised controlled trial to test the effect of an aerobic exercise intervention (AEI) on insulin parameters and body composition in non-obese BC women without insulin resistance. Thirty-eight BC women were randomised into an intervention group (IG = 18) or control group (CG = 20). IG participated in a structured AEI for 3 months, while CG received only the Word Cancer Research Fund/American Institute Cancer Research (WCRF/AICR) recommendation to be physically active. Fasting insulin, homeostasis model assessment of insulin resistance (HOMA-IR) index, metabolic parameters and body composition were collected at baseline and after the AEI. IG reduced insulin and HOMA-IR index by 15% and 14%, while CG increased these parameters (+12% and +16%). Insulin changed differently over time in the two randomised groups (pinteraction = .04). The between-group differences in the change of insulin (IG = −1.2 μU/ml versus CG = +0.8 μU/ml) and HOMA-IR index (IG = −0.26 versus CG = +0.25) were respectively significant (p = .04) and non-significant (p = .06). IG significantly improved lower limb muscle mass in comparison with CG (p = .03). A structured AEI may improve insulin, HOMA-IR index and body composition in non-obese BC survivors without insulin resistance.
References
- Abrahamson, P. E., Gammon, M. D., Lund, M. J., Flagg, E. W., Porter, P. L., Stevens, J., … & Coates, R. J. (2006). General and abdominal obesity and survival among young women with breast cancer. Cancer Epidemiology, Biomarkers and Prevention, 15, 1871–1877.
- Aleman-Mateo, H., Lopez Teros, M. T., Ramirez, F. A., & Astiazaran-Garcia, H. (2014). Association between insulin resistance and low relative appendicular skeletal muscle mass: Evidence from a cohort study in community-dwelling older men and women participants. The Journals of Gerontology. Series A, Biological Sciences and Medical Sciences, 69, 871–877.
- Bacigalupo, R., Cudd, P., Littlewood, C., Bissell, P., Hawley, M. S., & Buckley, W. H. (2013). Interventions employing mobile technology for overweight and obesity: An early systematic review of randomized controlled trials. Obesity Reviews, 14, 279–291.
- Ballard-Barbash, R., Friedenreich, C. M., Courneya, K. S., Siddiqi, S. M., McTiernan, A., & Alfano, C. M. (2012). Physical activity, biomarkers, and disease outcomes in cancer survivors: A systematic review. Journal of the National Cancer Institute, 104, 815–840.
- Beasley, J. M., Kwan, M. L., Chen, W. Y., Weltzien, E. K., Kroenke, C. H., Lu, W., … & Caan, B. J. (2012). Meeting the physical activity guidelines and survival after breast cancer: Findings from the after breast cancer pooling project. Breast Cancer Research and Treatment, 131, 637–643.
- Berrino, F., Villarini, A., Traina, A., Bonanni, B., Panico, S., Mano, M. P., … & Pasanisi, P. (2014). Metabolic syndrome and breast cancer prognosis. Breast Cancer Research and Treatment, 147, 159–165.
- Bruno, E., Gargano, G., Villarini, A., Traina, A., Johansson, H., Mano, M. P., … & Pasanisi, P. (2016). Adherence to WCRF/AICR cancer prevention recommendations and metabolic syndrome in breast cancer patients. International Journal of Cancer, 138, 237–244.
- Courneya, K. S., Segal, R. J., Mackey, J. R., Gelmon, K., Reid, R. D., Friedenreich, C. M., … & McKenzie, D. C. (2007). Effects of aerobic and resistance exercise in breast cancer patients receiving adjuvant chemotherapy: A multicenter randomized controlled trial. Journal of Clinical Oncology, 25, 4396–4404.
- DeNysschen, C. A., Brown, J. K., Cho, M. H., & Dodd, M. J. (2011). Nutritional symptom and body composition outcomes of aerobic exercise in women with breast cancer. Clinical Nursing Research, 20, 29–46.
- Drenowatz, C., Hand, G. A., Sagner, M., Shook, R. P., Burgess, S., & Blair, S. N. (2015). The prospective association between different types of exercise and body composition. Medicine and Science in Sports and Exercise, 47, 2535–2541.
- Fairey, A. S., Courneya, K. S., Field, C. J., Bell, G. J., Jones, L. W., & Mackey, J. R. (2003). 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 Epidemiology, Biomarkers and Prevention, 12, 721–727.
- Formica, V., Tesauro, M., Cardillo, C., & Roselli, M. (2012). Insulinemia and the risk of breast cancer and its relapse. Diabetes, Obesity and Metabolism, 14, 1073–1080.
- Frank, L. L., Sorensen, B. E., Yasui, Y., Tworoger, S. S., Schwartz, R. S., Ulrich, C. M., … & McTiernan, A. (2005). Effects of exercise on metabolic risk variables in overweight postmenopausal women: A randomized clinical trial. Obesity Research, 13, 615–625.
- Ghose, A., Kundu, R., Toumeh, A., Hornbeck, C., & Mohamed, I. (2015). A review of obesity, insulin resistance, and the role of exercise in breast cancer patients. Nutrition and Cancer, 67, 197–202.
- Giallauria, F., Maresca, L., Vitelli, A., De Santucci, M. M., Chiodini, P., Mattiello, A., … & Vigorito, C. (2015). Exercise training improves heart rate recovery in women with breast cancer. Springerplus, 4, 388.
- Giallauria, F., Vitelli, A., Maresca, L., De Santucci, M. M., Chiodini, P., Mattiello, A., … & Vigorito, C. (2016). Exercise training improves cardiopulmonary and endothelial function in women with breast cancer: Findings from the Diana-5 dietary intervention study. Internal and Emergency Medicine, 11, 183–189.
- Goodwin, P. J., Ennis, M., Pritchard, K. I., Trudeau, M. E., Koo, J., Madarnas, Y., … & Hood, N. (2002). Fasting insulin and outcome in early-stage breast cancer: Results of a prospective cohort study. Journal of Clinical Oncology, 20, 42–51.
- Goodwin, P. J., Ennis, M., Pritchard, K. I., Trudeau, M. E., Koo, J., Taylor, S. K., & Hood, N. (2012). Insulin- and obesity-related variables in early-stage breast cancer: Correlations and time course of prognostic associations. Journal of Clinical Oncology, 30, 164–171.
- Harris, J. A., & Benedict, F. G. (1918). A biometric study of human basal metabolism. Proceedings of the National Academy of Sciences of the United States of America, 4, 370–373.
- Hawley, J. A. (2004). Exercise as a therapeutic intervention for the prevention and treatment of insulin resistance. Diabetes/Metabolism Research and Reviews, 20, 383–393.
- Holick, C. N., Newcomb, P. A., Trentham-Dietz, A., Titus-Ernstoff, L., Bersch, A. J., Stampfer, M. J., … & Willett, W. C. (2008). Physical activity and survival after diagnosis of invasive breast cancer. Cancer Epidemiology, Biomarkers and Prevention, 17, 379–386.
- Holmes, M. D., Chen, W. Y., Feskanich, D., Kroenke, C. H., & Colditz, G. A. (2005). Physical activity and survival after breast cancer diagnosis. JAMA, 293, 2479–2486.
- Ibrahim, E. M., & Al-Homaidh, A. (2011). Physical activity and survival after breast cancer diagnosis: Meta-analysis of published studies. Medical Oncology, 28, 753–765.
- Irwin, M. L., Alvarez-Reeves, M., Cadmus, L., Mierzejewski, E., Mayne, S. T., Yu, H., … & Dipietro, L. (2009). Exercise improves body fat, lean mass, and bone mass in breast cancer survivors. Obesity(Silver Spring), 17, 1534–1541.
- Irwin, M. L., Varma, K., Alvarez-Reeves, M., Cadmus, L., Wiley, A., Chung, G. G., … & Yu, H. (2009). Randomized controlled trial of aerobic exercise on insulin and insulin-like growth factors in breast cancer survivors: The Yale Exercise and Survivorship study. Cancer Epidemiology, Biomarkers and Prevention, 18, 306–313.
- Jakicic, J. M., Marcus, M., Gallagher, K. I., Randall, C., Thomas, E., Goss, F. L., & Robertson, R. J. (2004). Evaluation of the SenseWear Pro Armband to assess energy expenditure during exercise. Medicine and Science in Sports and Exercise, 36, 897–904.
- Kleinberg, D. L., Wood, T. L., Furth, P. A., & Lee, A. V. (2009). Growth hormone and insulin-like growth factor-I in the transition from normal mammary development to preneoplastic mammary lesions. Endocrine Reviews, 30, 51–74.
- Knobf, M. T., Insogna, K., Dipietro, L., Fennie, C., & Thompson, A. S. (2008). An aerobic weight-loaded pilot exercise intervention for breast cancer survivors: Bone remodeling and body composition outcomes. Biological Research for Nursing, 10, 34–43.
- Lebrasseur, N. K., Achenbach, S. J., Melton, L. J. III, Amin, S., & Khosla, S. (2012). Skeletal muscle mass is associated with bone geometry and microstructure and serum insulin-like growth factor binding protein-2 levels in adult women and men. Journal of Bone and Mineral Research, 27, 2159–2169.
- Lewis, Z. H., Lyons, E. J., Jarvis, J. M., & Baillargeon, J. (2015). Using an electronic activity monitor system as an intervention modality: A systematic review. BMC Public Health, 15, 585.
- Ligibel, J. A., Campbell, N., Partridge, A., Chen, W. Y., Salinardi, T., Chen, H., … & Winer, E. P. (2008). Impact of a mixed strength and endurance exercise intervention on insulin levels in breast cancer survivors. Journal of Clinical Oncology, 26, 907–912.
- Lof, M., Bergstrom, K., & Weiderpass, E. (2012). Physical activity and biomarkers in breast cancer survivors: A systematic review. Maturitas, 73, 134–142.
- Lopez Teros, M. T., Ramirez, C. F., & Aleman-Mateo, H. (2015). Hyperinsulinemia is associated with the loss of appendicular skeletal muscle mass at 4.6 year follow-up in older men and women. Clinical Nutrition, 34, 931–936.
- Matthews, D. R., Hosker, J. P., Rudenski, A. S., Naylor, B. A., Treacher, D. F., & Turner, R. C. (1985). Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia, 28, 412–419.
- Pasanisi, P., Villarini, A., Bruno, E., Raimondi, M., Gargano, G., & Berrino, F. (2010). Nutritional advice to breast cancer survivors. Supportive Care in Cancer, 18(Suppl 2), S29–S33.
- Perez-Martin, A., Raynaud, E., & Mercier, J. (2001). Insulin resistance and associated metabolic abnormalities in muscle: Effects of exercise. Obesity Reviews, 2, 47–59.
- Rock, C. L., Doyle, C., Demark-Wahnefried, W., Meyerhardt, J., Courneya, K. S., Schwartz, A. L., … & Gansler, T. (2012). Nutrition and physical activity guidelines for cancer survivors. CA: A Cancer Journal for Clinicians, 62, 243–274.
- Roveda, E., Vitale, J. A., Bruno, E., Montaruli, A., Pasanisi, P., Villarini, A., … & Carandente, F. (2016). Protective effect of aerobic physical activity on sleep behavior in breast cancer survivors. Integrative Cancer Therapies, ePub. doi: 10.1177/1534735416651719
- Schmitz, K. H., Ahmed, R. L., Hannan, P. J., & Yee, D. (2005). Safety and efficacy of weight training in recent breast cancer survivors to alter body composition, insulin, and insulin-like growth factor axis proteins. Cancer Epidemiology, Biomarkers and Prevention, 14, 1672–1680.
- Schulz, K. F., Altman, D. G., & Moher, D. (2010). CONSORT 2010 statement: Updated guidelines for reporting parallel group randomised trials. BMJ, 340, c332.
- Shafer, K. J., Siders, W. A., Johnson, L. K., & Lukaski, H. C. (2009). Validity of segmental multiple-frequency bioelectrical impedance analysis to estimate body composition of adults across a range of body mass indexes. Nutrition, 25, 25–32.
- Shishikura, K., Tanimoto, K., Sakai, S., Tanimoto, Y., Terasaki, J., & Hanafusa, T. (2014). Association between skeletal muscle mass and insulin secretion in patients with type 2 diabetes mellitus. Endocrine Journal, 61, 281–287.
- Tanaka, H., Monahan, K. D., & Seals, D. R. (2001). Age-predicted maximal heart rate revisited. Journal of the American College of Cardiology, 37, 153–156.
- van, H. K., Mortelmans, P., & Lefevre, J. (2014). Validation of the SenseWear Pro3 Armband using an incremental exercise test. Journal of Strength and Conditioning Research, 28, 2806–2814.
- Villarini, A., Pasanisi, P., Traina, A., Mano, M. P., Bonanni, B., Panico, S., … & Berrino, F. (2012). Lifestyle and breast cancer recurrences: The DIANA-5 trial. Tumori, 98, 1–18.
- Villasenor, A., Ballard-Barbash, R., Baumgartner, K., Baumgartner, R., Bernstein, L., McTiernan, A., & Neuhouser, M. L. (2012). Prevalence and prognostic effect of sarcopenia in breast cancer survivors: The HEAL Study. Journal of Cancer Survivorship, 6, 398–406.
- World Cancer Research Fund. (2014). Diet, nutrition, physical acivity and breast cancer survivors. Available from: http://www.wcrf.org/sites/default/files/Breast-Cancer-Survivors-2014-Report.pdf. [last accessed 25 August 2016]
- World Cancer Research Fund & American Institute for Cancer Research. (2007). Food, nutrition, physical activity and the prevention of cancer: A global perspective. Washington, DC: AICR.
- Wu, Y., Zhang, D., & Kang, S. (2013). Physical activity and risk of breast cancer: A meta-analysis of prospective studies. Breast Cancer Research and Treatment, 137, 869–882.
- Zhong, S., Jiang, T., Ma, T., Zhang, X., Tang, J., Chen, W., Lv, M., & Zhao, J. (2014). Association between physical activity and mortality in breast cancer: A meta-analysis of cohort studies. European Journal of Epidemiology, 29, 391–404.