Top

Published in:

01-06-2020 | Breast Cancer | Original Article

Exercise type and fat mass loss regulate breast cancer-related sex hormones in obese and overweight postmenopausal women

Authors: Paola Gonzalo-Encabo, David Valadés, Natalio García-Honduvilla, Ana de Cos Blanco, Christine M. Friedenreich, Alberto Pérez-López

Published in: European Journal of Applied Physiology | Issue 6/2020

Abstract

Purpose

The aim of the study was to examine the effects of a time-matched endurance versus concurrent training on circulating sex hormone levels and body composition in postmenopausal women.

Methods

Thirty-five sedentary and obese postmenopausal women were recruited and randomly divided into endurance training (EN, n = 10), concurrent training (CON, n = 13), or control group (C, n = 12). Participants took part in a 12-week supervised intervention, training 3 days/week and 60 min/session. Before and after the intervention, body composition was assessed, and blood samples were obtained to evaluate estradiol, testosterone, DHEA-S, and SHBG.

Result

In response to training, a reduction in total fat mass was found (5.3%; P < 0.05), while an increase in lean body mass was observed in the CON group (1.5%; P < 0.05). There was a significant decrease in DHEA-S (− 13%), total (− 40%) and free testosterone (− 41%) in the EN group, while in the CON group, total (25%) and free testosterone (21%) increased significantly (P < 0.05). When participants were stratified according to fat mass loss (> or < 2 kg), a statistically significant increase in circulating SHBG (21%) and decrease in DHEA-S (− 13%) were found.

Conclusion

The type of exercise and exercise-induced fat mass loss seem to modify the sex hormone profile in postmenopausal women that is an established risk factor of breast cancer. Thus, this study provides additional evidences to the intricated interaction among sex hormones, adipose tissue, and muscle mass in postmenopausal women.

Available only for authorised users

Adraskela K, Veisaki E, Koutsilieris M, Philippou A (2017) Physical exercise positively influences breast cancer evolution. Clin Breast Cancer 17:408–417. https://doi.org/10.1016/j.clbc.2017.05.003 CrossRefPubMed

American College of Sports Medicine (ACSM) (2000) ACSM’s guidelines for exercise testing and prescription, vol 8. Lippincott Williams & Wilkins, Philadelphia

American College of Sports Medicine (ACSM) (2009) American college of sports medicine position stand. progression models in resistance training for healthy adults. Med Sci Sports Exerc 41:687–708. https://doi.org/10.1249/MSS.0b013e3181915670 CrossRef

Baulieu EE (1996) Dehydroepiandrosterone (DHEA): a fountain of youth? J Clin Endocrinol Metab 81:3147–3151. https://doi.org/10.1210/jcem.81.9.8784058 CrossRefPubMed

Campbell KL et al (2012) Reduced-calorie dietary weight loss, exercise, and sex hormones in postmenopausal women: randomized controlled trial. J Clin Oncol 30:2314–2326. https://doi.org/10.1200/JCO.2011.37.9792 CrossRefPubMedPubMedCentral

Cleary MP, Grossmann ME (2009) Minireview: obesity and breast cancer: the estrogen connection. Endocrinology 150:2537–2542. https://doi.org/10.1210/en.2009-0070 CrossRefPubMedPubMedCentral

Corbould AM, Judd SJ, Rodgers RJ (1998) Expression of types 1, 2, and 3 17 beta-hydroxysteroid dehydrogenase in subcutaneous abdominal and intra-abdominal adipose tissue of women. J Clin Endocrinol Metab 83:187–194. https://doi.org/10.1210/jcem.83.1.4495 CrossRefPubMed

Costantino JP, Gail MH, Pee D, Anderson S, Redmond CK, Benichou J, Wieand HS (1999) Validation studies for models projecting the risk of invasive and total breast cancer incidence. J Natl Cancer Inst 91:1541–1548. https://doi.org/10.1093/jnci/91.18.1541 CrossRefPubMed

Craig CL et al (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35:1381–1395. https://doi.org/10.1249/01.MSS.0000078924.61453.FB CrossRefPubMed

de Roon M, May AM, McTiernan A, Scholten R, Peeters PHM, Friedenreich CM, Monninkhof EM (2018) Effect of exercise and/or reduced calorie dietary interventions on breast cancer-related endogenous sex hormones in healthy postmenopausal women. Breast Cancer Res 20:81. https://doi.org/10.1186/s13058-018-1009-8 CrossRefPubMedPubMedCentral

Dieterich M, Stubert J, Reimer T, Erickson N, Berling A (2014) Influence of lifestyle factors on breast cancer risk. Breast Care (Basel) 9:407–414. https://doi.org/10.1159/000369571 CrossRef

Dimitrakakis C et al (2003) A physiologic role for testosterone in limiting estrogenic stimulation of the breast. Menopause 10:292–298. https://doi.org/10.1097/01.GME.0000055522.67459.89 CrossRefPubMed

Dunnett CW (1980) Pairwise multiple comparisons in the homogeneous variance, unequeal sample size case. J Am Stat Assoc 75(372):789–795. https://doi.org/10.2307/2287160 CrossRef

Ennour-Idrissi K, Maunsell E, Diorio C (2015) Effect of physical activity on sex hormones in women: a systematic review and meta-analysis of randomized controlled trials. Breast Cancer Res 17:139. https://doi.org/10.1186/s13058-015-0647-3 CrossRefPubMedPubMedCentral

Friedenreich CM (2010a) The role of physical activity in breast cancer etiology. Semin Oncol 37:297–302. https://doi.org/10.1053/j.seminoncol.2010.05.008 CrossRefPubMed

Friedenreich CM et al (2015) Effects of exercise dose on endogenous estrogens in postmenopausal women: a randomized trial. Endocr Relat Cancer 22:863–876. https://doi.org/10.1530/ERC-15-0243 CrossRefPubMed

Friedenreich CM et al (2010) Alberta physical activity and breast cancer prevention trial: sex hormone changes in a year-long exercise intervention among postmenopausal women. J Clin Oncol 28:1458–1466. https://doi.org/10.1200/JCO.2009.24.9557 CrossRefPubMedPubMedCentral

Garber CE et al (2011) 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 43:1334–1359. https://doi.org/10.1249/MSS.0b013e318213fefb CrossRefPubMed

Glaser R, Dimitrakakis C (2013) Testosterone therapy in women: myths and misconceptions. Maturitas 74:230–234. https://doi.org/10.1016/j.maturitas.2013.01.003 CrossRefPubMed

Goldberg DP, Hillier VF (1979) A scaled version of the general health questionnaire. Psychol Med 9:139–145CrossRef

Gonzalo-Encabo P, Valadés D, De Cos AI, García-Honduvilla N, Pérez-López A (2019) Effects of exercise on circulating levels of sex hormones in overweight and obese postmenopausal women: a systematic review. Sci Sports. https://doi.org/10.1016/j.scispo.2018.09.012 CrossRef

Haskell WL, Lee IM, Pate RR, Powell KE, Blair SN, Franklin BA et al (2007) Physical activity and public health: updated recommendation for adults from the American college of sports medicine and the American heart association. Med Sci Sports Exerc 39(8):1423–1434. https://doi.org/10.1249/mss.0b013e3180616b27 CrossRefPubMed

He Z, Rankinen T, Leon AS, Skinner JS, Tchernof A, Bouchard C (2018) Plasma steroids, body composition, and fat distribution: effects of age, sex, and exercise training. Int J Obes (Lond) 42:1366–1377. https://doi.org/10.1038/s41366-018-0033-1 CrossRef

Kaaks R et al (2005) Postmenopausal serum androgens, oestrogens and breast cancer risk: the European prospective investigation into cancer and nutrition. Endocr Relat Cancer 12:1071–1082. https://doi.org/10.1677/erc.1.01038 CrossRefPubMed

Kendall A, Folkerd EJ, Dowsett M (2007) Influences on circulating oestrogens in postmenopausal women: relationship with breast cancer. J Steroid Biochem Mol Biol 103:99–109. https://doi.org/10.1016/j.jsbmb.2006.07.011 CrossRefPubMed

Key T, Appleby P, Barnes I, Reeves G, Endogenous H, Breast Cancer Collaborative G (2002) Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J Natl Cancer Inst 94:606–616CrossRef

Liu CH, Laughlin GA, Fischer UG, Yen SS (1990) Marked attenuation of ultradian and circadian rhythms of dehydroepiandrosterone in postmenopausal women: evidence for a reduced 17,20-desmolase enzymatic activity. J Clin Endocrinol Metab 71:900–906. https://doi.org/10.1210/jcem-71-4-900 CrossRefPubMed

Mayhew JLBT, Arnold TE, Bowen JC (1992) Relative muscular endurance as a predictor of bench press in college men and women. J Appl Sports Sci Res 6:200–206

McTiernan A et al (2004a) Effect of exercise on serum androgens in postmenopausal women: a 12-month randomized clinical trial. Cancer Epidemiol Biomarkers Prev 13:1099–1105PubMed

McTiernan A et al (2004b) Effect of exercise on serum estrogens in postmenopausal women: a 12-month randomized clinical trial. Cancer Res 64:2923–2928CrossRef

Monninkhof EM et al (2007) Physical activity and breast cancer: a systematic review. Epidemiology 18:137–157. https://doi.org/10.1097/01.ede.0000251167.75581.98 CrossRefPubMed

Monninkhof EM, Velthuis MJ, Peeters PH, Twisk JW, Schuit AJ (2009) Effect of exercise on postmenopausal sex hormone levels and role of body fat: a randomized controlled trial. J Clin Oncol 27:4492–4499. https://doi.org/10.1200/JCO.2008.19.7459 CrossRefPubMed

Munsell MF, Sprague BL, Berry DA, Chisholm G, Trentham-Dietz A (2014) Body mass index and breast cancer risk according to postmenopausal estrogen-progestin use and hormone receptor status. Epidemiol Rev 36:114–136. https://doi.org/10.1093/epirev/mxt010 CrossRefPubMedPubMedCentral

Neilson HK, Conroy SM, Friedenreich CM (2014) The influence of energetic factors on biomarkers of postmenopausal breast cancer risk. Curr Nutr Rep 3:22–34. https://doi.org/10.1007/s13668-013-0069-8 CrossRefPubMed

Notelovitz M (2002) Androgen effects on bone and muscle. Fertil Steril 77(Suppl 4):S34–41CrossRef

Orsatti FL, Nahas EA, Maesta N, Nahas-Neto J, Burini RC (2008) Plasma hormones, muscle mass and strength in resistance-trained postmenopausal women. Maturitas 59:394–404. https://doi.org/10.1016/j.maturitas.2008.04.002 CrossRefPubMed

Parker CR Jr, Slayden SM, Azziz R, Crabbe SL, Hines GA, Boots LR, Bae S (2000) Effects of aging on adrenal function in the human: responsiveness and sensitivity of adrenal androgens and cortisol to adrenocorticotropin in premenopausal and postmenopausal women. J Clin Endocrinol Metab 85:48–54. https://doi.org/10.1210/jcem.85.1.6265 CrossRefPubMed

Pérez-López A, Valades D, de Cos Blanco AI, Garcia-Honduvilla N, Vazquez Martinez C (2019) Circulating adiponectin expression is elevated and associated with the IL-15/IL-15Ralpha complex in obese physically active humans. J Sports Med Phys Fitness 59:1229–1237. https://doi.org/10.23736/S0022-4707.18.09030-8 CrossRefPubMed

Pérez-López A, Valades D, Vazquez Martinez C, de Cos Blanco AI, Bujan J, Garcia-Honduvilla N (2018) Serum IL-15 and IL-15Ralpha levels are decreased in lean and obese physically active humans. Scand J Med Sci Sports 28:1113–1120. https://doi.org/10.1111/sms.12983 CrossRefPubMed

Rinaldi S et al (2001) Reliability and validity of commercially available, direct radioimmunoassays for measurement of blood androgens and estrogens in postmenopausal women. Cancer Epidemiol Biomarkers Prev 10:757–765PubMed

Rinaldi S et al (2002) Validity of free testosterone and free estradiol determinations in serum samples from postmenopausal women by theoretical calculations. Cancer Epidemiol Biomarkers Prev 11:1065–1071PubMed

Schmidt S, Monk JM, Robinson LE, Mourtzakis M (2015) The integrative role of leptin, oestrogen and the insulin family in obesity-associated breast cancer: potential effects of exercise. Obes Rev 16:473–487. https://doi.org/10.1111/obr.12281 CrossRefPubMedPubMedCentral

van Gemert WA et al (2017) Association between changes in fat distribution and biomarkers for breast cancer. Endocr Relat Cancer 24:297–305. https://doi.org/10.1530/ERC-16-0490 CrossRefPubMed

van Gemert WA et al (2015) Effect of weight loss, with or without exercise, on body composition and sex hormones in postmenopausal women: the SHAPE-2 trial. Breast Cancer Res 17:120. https://doi.org/10.1186/s13058-015-0633-9 CrossRefPubMedPubMedCentral

Yager JD, Davidson NE (2006) Estrogen carcinogenesis in breast cancer. N Engl J Med 354:270–282. https://doi.org/10.1056/NEJMra050776 CrossRefPubMed

Zang H, Ryden M, Wahlen K, Dahlman-Wright K, Arner P, Linden Hirschberg A (2007) Effects of testosterone and estrogen treatment on lipolysis signaling pathways in subcutaneous adipose tissue of postmenopausal women. Fertil Steril 88:100–106. https://doi.org/10.1016/j.fertnstert.2006.11.088 CrossRefPubMed

Title: Exercise type and fat mass loss regulate breast cancer-related sex hormones in obese and overweight postmenopausal women
Authors: Paola Gonzalo-Encabo
David Valadés
Natalio García-Honduvilla
Ana de Cos Blanco
Christine M. Friedenreich
Alberto Pérez-López
Publication date: 01-06-2020
Publisher: Springer Berlin Heidelberg
Keywords: Breast Cancer
Breast Cancer
Overweight
Testosterone
Androgens
Estrogens
Estradiol
Published in: European Journal of Applied Physiology / Issue 6/2020
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-020-04361-1

At a glance: The STEP trials

Springer Medicine

Exercise type and fat mass loss regulate breast cancer-related sex hormones in obese and overweight postmenopausal women

Abstract

Purpose

Methods

Result

Conclusion

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Methods

Result

Conclusion

Please log in to get access to this content

Other articles of this Issue 6/2020

On the climbing performance enhancing effects of New Zealand blackcurrant extract

Dietary nitrate does not acutely enhance skeletal muscle blood flow and vasodilation in the lower limbs of older adults during single-limb exercise

A model-based estimation of critical torques reduces the experimental effort compared to conventional testing

Neuromuscular function and fatigability in people diagnosed with head and neck cancer before versus after treatment

Acute physiological responses to combined blood flow restriction and low-level laser

Acute hypertrophic but not maximal strength loading transiently enhances the kynurenine pathway towards kynurenic acid