The Effect of Exercise Training on Serum Glucose and Lipid Profiles in Patients With Breast Cancer: A Systematic Review and Meta-Analysis of Randomized Clinical Trials

in Journal of Physical Activity and Health
Restricted access

Purchase article

USD  $24.95

Student 1 year online subscription

USD  $119.00

1 year online subscription

USD  $159.00

Student 2 year online subscription

USD  $227.00

2 year online subscription

USD  $302.00

Background: Despite several studies on the effects of exercise training on glucose and lipid profiles in patients with breast cancer, no earlier study has systematically summarized their findings. Current systematic review and meta-analysis have been done on earlier clinical trials in this topic. Methods: Relevant studies published up to May 2020 were searched through PubMed, SCOPUS, and Google Scholar using predefined keywords. Studies that examined the effect of exercise training on serum glucose and lipid profiles in adult women with breast cancer were included. Results: A total of 16 studies were included. Combining 10 effect sizes, exercise training had no significant influence on serum fasting plasma glucose concentrations (weighted mean difference [WMD] = 4.87; 95% confidence interval [CI], −4.65 to 14.29). However, it resulted in significant reduction of serum insulin (WMD = −2.37; 95% CI, −3.57 to −1.16) and homeostatic model assessment for insulin resistance (WMD = −0.71; 95% CI, −1.27 to −0.15) in 14 and 8 studies, respectively. Pooling 6 effect sizes, exercise training did not change serum total cholesterol (WMD = −11.99; 95% CI, −32.42 to 8.45), low-density lipoprotein (WMD = −3.21; 95% CI, −10.45 to 4.04), high-density lipoprotein (WMD = 4.13; 95% CI, −6.20 to 14.46), and triglyceride (WMD = −23.34; 95% CI, −66.96 to 20.29) concentrations. Subgroup analyses showed beneficial effects of exercise training on outcomes of interest among studies with higher methodological quality. Conclusion: Current meta-analysis demonstrated significant reductions in serum levels of insulin and insulin resistance following exercise training. However, exercise training had no significant effect on serum levels of fasting plasma glucose, total cholesterol, triglyceride, high-density lipoprotein, and low-density lipoprotein. Further high-quality studies are needed to shed light on this issue.

Abbasi and Eslami are with the Department of Sport Injuries, Faculty of Physical Education and Sport Sciences, Allameh Tabataba’i University, Tehran, Iran. Khademi is with the Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran. Milajerdi is with the Research Center for Biochemistry and Nutrition in Metabolic Diseases, Institute for Basic Sciences, Kashan University of Medical Sciences, Kashan, Iran; and the Department of Health, Science and Research Branch, AJA University of Medical Sciences, Tehran, Iran.

Eslami (eslami.rasul@gmail.com) and Milajerdi (amkhv@yahoo.com) are corresponding authors.

Supplementary Materials

    • Supplementary Table S1 (PDF 278 KB)
    • Supplementary Table S2 (PDF 196 KB)
  • 1.

    Torre LA, Islami F, Siegel RL, Ward EM, Jemal A. Global cancer in women: burden and trends. Cancer Epidemiol Biomarkers Prev. 2017;26(4):444–57.

    • Search Google Scholar
    • Export Citation
  • 2.

    Li P, Wang T, Zeng C, et al. . Association between metabolic syndrome and prognosis of breast cancer: a meta-analysis of follow-up studies. Diabetes Metab Syndr. 2020;12(1):10. doi:10.1186/s13098-019-0514-y

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 3.

    Anastasiadi Z, Lianos GD, Ignatiadou E, Harissis HV, Mitsis M. Breast cancer in young women: an overview. Updates Surg. 2017;69(3):313317. PubMed ID: 28260181 doi:10.1007/s13304-017-0424-1

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    He J, Gu Y, Zhang S. Vitamin A and breast cancer survival: a systematic review and meta-analysis. Clin Breast Cancer. 2018;18(6):e1389e400. PubMed ID: 30190194 doi:10.1016/j.clbc.2018.07.025

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Anjom-Shoae J, Sadeghi O, Larijani B, Esmaillzadeh A. Dietary intake and serum levels of trans fatty acids and risk of breast cancer: a systematic review and dose-response meta-analysis of prospective studies. Clin Nutr. 2020;39(3):755764. PubMed ID: 30954361 doi:10.1016/j.clnu.2019.03.024

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Leris C, Mokbel K. The prevention of breast cancer: an overview. Curr Med Res Opin. 2000;16(4):252257. doi:10.1185/0300799019117004

  • 7.

    Milajerdi A, Namazi N, Larijani B, Azadbakht L. The association of dietary quality indices and cancer mortality: a systematic review and meta-analysis of cohort studies. Nutr Cancer. 2018;70(7):10911105. PubMed ID: 30321058 doi:10.1080/01635581.2018.1502331

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Loprinzi PD, Cardinal BJ. Effects of physical activity on common side effects of breast cancer treatment. Breast Cancer. 2012;19(1):410. PubMed ID: 21725654 doi:10.1007/s12282-011-0292-3

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Bruun JM, Helge JW, Richelsen B, Stallknecht B. Diet and exercise reduce low-grade inflammation and macrophage infiltration in adipose tissue but not in skeletal muscle in severely obese subjects. Am J Physiol Endocrinol Metab. 2006;290(5):E961E967. PubMed ID: 16352667 doi:10.1152/ajpendo.00506.2005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Ashtary-Larky D, Lamuchi-Deli N, Milajerdi A, et al. . Inflammatory and biochemical biomarkers in response to high intensity resistance training in trained and untrained men. Asian J Sports Med. 2017;8(2):1–8.

    • Search Google Scholar
    • Export Citation
  • 11.

    Ertunc ME, Hotamisligil GS. Lipid signaling and lipotoxicity in metaflammation: indications for metabolic disease pathogenesis and treatment. J Lipid Res. 2016;57(12):20992114. PubMed ID: 27330055 doi:10.1194/jlr.R066514

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Kang D-W, Lee J, Suh S-H, Ligibel J, Courneya KS, Jeon JY. Effects of exercise on insulin, IGF axis, adipocytokines, and inflammatory markers in breast cancer survivors: a systematic review and meta-analysis. Cancer Epidemiol Biomark Prev. 2017;26(3):355365. doi:10.1158/1055-9965.EPI-16-0602

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13.

    Dash C, Taylor TR, Makambi KH, Hicks J, Hagberg JM, Adams‐Campbell LL. Effect of exercise on metabolic syndrome in black women by family history and predicted risk of breast cancer: The FIERCE Study. Cancer. 2018;124(16):33553363. PubMed ID: 29975403 doi:10.1002/cncr.31569

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    de Paulo TR, Winters-Stone KM, Viezel J, et al. . Effects of resistance plus aerobic training on body composition and metabolic markers in older breast cancer survivors undergoing aromatase inhibitor therapy. Exp Gerontol. 2018;111:210217. PubMed ID: 30077574 doi:10.1016/j.exger.2018.07.022

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Bruno E, Roveda E, Vitale J, et al. . Effect of aerobic exercise intervention on markers of insulin resistance in breast cancer women. Eur J Cancer Care. 2018;27(2):e12617. doi:10.1111/ecc.12617

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Dieli-Conwright CM, Courneya KS, Demark-Wahnefried W, et al. . Effects of aerobic and resistance exercise on metabolic syndrome, sarcopenic obesity, and circulating biomarkers in overweight or obese survivors of breast cancer: a randomized controlled trial. J Clin Oncol 2018;36(9):875. PubMed ID: 29356607 doi:10.1200/JCO.2017.75.7526

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    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 Biomark Prev. 2003;12(8):7217.

    • Search Google Scholar
    • Export Citation
  • 18.

    Fairey AS, Courneya KS, Field CJ, et al. . Effect of exercise training on C-reactive protein in postmenopausal breast cancer survivors: a randomized controlled trial. Brain Behav Immun. 2005;19(5):381388. PubMed ID: 15922556 doi:10.1016/j.bbi.2005.04.001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Guinan E, Hussey J, Broderick J, et al. . The effect of aerobic exercise on metabolic and inflammatory markers in breast cancer survivors—a pilot study. Support Care Cancer. 2013;21(7):19831992. PubMed ID: 23430010 doi:10.1007/s00520-013-1743-5

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Irwin ML, Varma K, Alvarez-Reeves M, et al. . 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 Biomark Prev. 2009;18(1):306313. doi:10.1158/1055-9965.EPI-08-0531

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Janelsins MC, Davis PG, Wideman L, et al. . Effects of Tai Chi Chuan on insulin and cytokine levels in a randomized controlled pilot study on breast cancer survivors. Clin Breast Cancer. 2011;11(3):161170. PubMed ID: 21665136 doi:10.1016/j.clbc.2011.03.013

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22.

    Lahart IM, Metsios GS, Nevill AM, Kitas GD, Carmichael AR. Randomised controlled trial of a home-based physical activity intervention in breast cancer survivors. BMC Cancer. 2016;16(1):234. doi:10.1186/s12885-016-2258-5

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Ligibel JA, Campbell N, Partridge A, et al. . Impact of a mixed strength and endurance exercise intervention on insulin levels in breast cancer survivors. J Clin Oncol. 2008;26(6):907912. PubMed ID: 18281663 doi:10.1200/JCO.2007.12.7357

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Ligibel JA, Dillon D, Giobbie-Hurder A, et al. . Impact of a pre-operative exercise intervention on breast cancer proliferation and gene expression: results from the Pre-Operative Health and Body (PreHAB) Study. Clin Cancer Res. 2019;25(17):53985406. PubMed ID: 31018921 doi:10.1158/1078-0432.CCR-18-3143

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Nuri R, Kordi MR, Moghaddasi M, et al. . Effect of combination exercise training on metabolic syndrome parameters in postmenopausal women with breast cancer. J Cancer Res Ther. 2012;8(2):238. PubMed ID: 22842368 doi:10.4103/0973-1482.98977

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Schmitz KH, Ahmed RL, Hannan PJ, Yee D. Safety and efficacy of weight training in recent breast cancer survivors to alter body composition, insulin, and insulin-like growth factor axis proteins. Cancer Epidemiol Biomark Prev. 2005;14(7):16721680. doi:10.1158/1055-9965.EPI-04-0736

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Sprod LK, Janelsins MC, Palesh OG, et al. . Health-related quality of life and biomarkers in breast cancer survivors participating in tai chi chuan. J Cancer Surviv. 2012;6(2):146154. PubMed ID: 22160628 doi:10.1007/s11764-011-0205-7

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Winters-Stone KM, Wood LJ, Stoyles S, Dieckmann NF. The effects of resistance exercise on biomarkers of breast cancer prognosis: a pooled analysis of three randomized trials. Cancer Epidemiol Biomark Prev. 2018;27(2):146153. doi:10.1158/1055-9965.EPI-17-0766

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    Kim TH, Chang JS, Park K-S, et al. . Effects of exercise training on circulating levels of Dickkpof-1 and secreted frizzled-related protein-1 in breast cancer survivors: a pilot single-blind randomized controlled trial. PLoS One. 2017;12(2):e0171771. PubMed ID: 28178355 doi:10.1371/journal.pone.0171771

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Wang Y, Jin B, Paxton RJ, et al. . The effects of exercise on insulin, glucose, IGF‐axis and CRP in cancer survivors: meta‐analysis and meta‐regression of randomised controlled trials. Eur J Cancer. 2020;29(1):e13186. doi:10.1111/ecc.13186

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Brown JC, Rickels MR, Troxel AB, et al. . Dose–response effects of exercise on insulin among colon cancer survivors. Endocr-Relat Cancer. 2018;25(1):1119. PubMed ID: 29018055 doi:10.1530/ERC-17-0377

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Dawson JK, Dorff TB, Schroeder ET, Lane CJ, Gross ME, Dieli-Conwright CM. Impact of resistance training on body composition and metabolic syndrome variables during androgen deprivation therapy for prostate cancer: a pilot randomized controlled trial. BMC Cancer. 2018;18(1):368. PubMed ID: 29614993 doi:10.1186/s12885-018-4306-9

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    Lee MK, Kim J-Y, Kim D-I, et al. . Effect of home-based exercise intervention on fasting insulin and adipocytokines in colorectal cancer survivors: a randomized controlled trial. Metabolism. 2017;76:2331. PubMed ID: 28987237 doi:10.1016/j.metabol.2017.07.005

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Papadopoulos E, Santa Mina D, Culos-Reed N, et al. . Effects of six months of aerobic and resistance training on metabolic markers and bone mineral density in older men on androgen deprivation therapy for prostate cancer. J Geriatr Oncol. 2020;11(7):1074–7.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Karlsson HK, Zierath JR. Insulin signaling and glucose transport in insulin resistant human skeletal muscle. Cell Biochem Biophys. 2007;48(2–3):103113. PubMed ID: 17709880 doi:10.1007/s12013-007-0030-9

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Carlson C, Winder W. Liver AMP-activated protein kinase and acetyl-CoA carboxylase during and after exercise. J Appl Physiol. 1999;86(2):669674. PubMed ID: 9931206 doi:10.1152/jappl.1999.86.2.669

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Gunter MJ, Hoover DR, Yu H, et al. . Insulin, insulin-like growth factor-I, and risk of breast cancer in postmenopausal women. J Natl Cancer Inst. 2009;101(1):4860. PubMed ID: 19116382 doi:10.1093/jnci/djn415

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Van Der Heijden G-j, Wang ZJ, Chu Z, et al. . Strength exercise improves muscle mass and hepatic insulin sensitivity in obese youth. Med Sci Sports Exerc. 2010;42(11):1973. doi:10.1249/MSS.0b013e3181df16d9

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 39.

    Ivy JL. Role of exercise training in the prevention and treatment of insulin resistance and non-insulin-dependent diabetes mellitus. Sports Med. 1997;24(5):321336. PubMed ID: 9368278 doi:10.2165/00007256-199724050-00004

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Balducci S, Zanuso S, Nicolucci A, et al. . Anti-inflammatory effect of exercise training in subjects with type 2 diabetes and the metabolic syndrome is dependent on exercise modalities and independent of weight loss. Nutr Metab Cardiovasc Dis. 2010;20(8):608617. doi:10.1016/j.numecd.2009.04.015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 41.

    Milajerdi A, Larijani B, Esmaillzadeh A. Statins influence biomarkers of low grade inflammation in apparently healthy people or patients with chronic diseases: a systematic review and meta-analysis of randomized clinical trials. Cytokine. 2019;123:154752. PubMed ID: 31228727 doi:10.1016/j.cyto.2019.154752

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Mulya A, Haus JM, Solomon TP, et al. . Exercise training‐induced improvement in skeletal muscle PGC‐1α‐mediated fat metabolism is independent of dietary glycemic index. Obesity. 2017;25(4):721729. PubMed ID: 28349667 doi:10.1002/oby.21799

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Nieuwoudt S, Fealy CE, Foucher JA, et al. . Functional high-intensity training improves pancreatic β-cell function in adults with type 2 diabetes. Am J Physiol Endocrinol Metab. 2017;313(3):E314E20. PubMed ID: 28512155 doi:10.1152/ajpendo.00407.2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Solomon TP, Haus JM, Kelly KR, Rocco M, Kashyap SR, Kirwan JP. Improved pancreatic β-cell function in type 2 diabetic patients after lifestyle-induced weight loss is related to glucose-dependent insulinotropic polypeptide. Diabetes Care. 2010;33(7):15611566. PubMed ID: 20200305 doi:10.2337/dc09-2021

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 683 683 335
Full Text Views 17 17 0
PDF Downloads 18 18 0