Impact of a Pre-Operative Exercise Intervention on Breast Cancer Proliferation and Gene Expression: Results from the Pre-Operative Health and Body (PreHAB) Study

Purpose: Exercise after breast cancer diagnosis is associated with lower cancer-specific mortality, but the biological mechanisms through which exercise impacts breast cancer are not fully understood. The Pre-Operative Health and Body (PreHAB) Study was a randomized window-of-opportunity trial designed to test the impact of exercise on Ki-67, gene expression, and other biomarkers in women with breast cancer. Experimental Design: Inactive women with newly diagnosed breast cancer were randomized to an exercise intervention or mind–body control group, and participated in the study between enrollment and surgery (mean 29.3 days). Tumor and serum were collected at baseline and surgery. Results: Forty-nine women were randomized (27 exercise, 22 control). At baseline, mean age was 52.6, body mass index was 30.2 kg/m2, and exercise was 49 minutes/week. Exercise participants significantly increased exercise versus controls (203 vs. 23 minutes/week, P < 0.0001). There were no differences in changes of expression of Ki-67, insulin receptor, and cleaved caspase-3 in exercise participants versus controls. KEGG pathway analysis demonstrated significant upregulation of 18 unique pathways between the baseline biopsy and surgical excision in exercise participants and none in control participants (q < 0.1). Top-ranked pathways included several implicated in immunity and inflammation. Exploratory analysis of tumor immune infiltrates demonstrated a trend toward a decrease in FOXP3+ cells in exercise versus control participants over the intervention period (P = 0.08). Conclusions: A window-of-opportunity exercise intervention did not impact proliferation but led to alterations in gene expression in breast tumors, suggesting that exercise may have a direct effect on breast cancer. See related commentary by Koelwyn and Jones, p. 5179

[1]  Bo Li,et al.  VIPER: Visualization Pipeline for RNA-seq, a Snakemake workflow for efficient and complete RNA-seq analysis , 2018, BMC Bioinformatics.

[2]  J. Ioannidis,et al.  Physical activity and cancer: an umbrella review of the literature including 22 major anatomical sites and 770 000 cancer cases , 2017, British Journal of Sports Medicine.

[3]  R. White,et al.  Exercise-dependent regulation of the tumour microenvironment , 2017, Nature Reviews Cancer.

[4]  Heather K. Neilson,et al.  Moderate-vigorous recreational physical activity and breast cancer risk, stratified by menopause status: a systematic review and meta-analysis , 2017, Menopause.

[5]  P. Hojman,et al.  Exercise-Dependent Regulation of NK Cells in Cancer Protection. , 2016, Trends in molecular medicine.

[6]  I. Nookaew,et al.  Voluntary Running Suppresses Tumor Growth through Epinephrine- and IL-6-Dependent NK Cell Mobilization and Redistribution. , 2016, Cell metabolism.

[7]  C. Gross,et al.  Randomized exercise trial of aromatase inhibitor-induced arthralgia in breast cancer survivors. , 2015, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[8]  J. Christensen,et al.  Effects of Exercise on Tumor Physiology and Metabolism , 2015, Cancer journal.

[9]  G. Pond,et al.  Evaluating the Feasibility of Performing Window of Opportunity Trials in Breast Cancer , 2015, International journal of surgical oncology.

[10]  W. Huber,et al.  Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 , 2014, Genome Biology.

[11]  S. Zhong,et al.  Association between physical activity and mortality in breast cancer: a meta-analysis of cohort studies , 2014, European Journal of Epidemiology.

[12]  D. Abdalla,et al.  Innate immune response adaptation in mice subjected to administration of DMBA and physical activity , 2013, Oncology letters.

[13]  Thomas R. Gingeras,et al.  STAR: ultrafast universal RNA-seq aligner , 2013, Bioinform..

[14]  Sameer M. Siddiqi,et al.  Physical activity, biomarkers, and disease outcomes in cancer survivors: a systematic review. , 2012, Journal of the National Cancer Institute.

[15]  Weiqin Jiang,et al.  Effects of Energy Restriction and Wheel Running on Mammary Carcinogenesis and Host Systemic Factors in a Rat Model , 2012, Cancer Prevention Research.

[16]  A. McTiernan,et al.  Wheel Running–Induced Changes in Plasma Biomarkers and Carcinogenic Response in the 1-Methyl-1-Nitrosourea–Induced Rat Model for Breast Cancer , 2010, Cancer Prevention Research.

[17]  K. Courneya,et al.  American College of Sports Medicine roundtable on exercise guidelines for cancer survivors. , 2010, Medicine and science in sports and exercise.

[18]  Cole Trapnell,et al.  Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. , 2010, Nature biotechnology.

[19]  Weiqin Jiang,et al.  Effects of Physical Activity and Restricted Energy Intake on Chemically Induced Mammary Carcinogenesis , 2009, Cancer Prevention Research.

[20]  L. DiPietro,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 , 2009, Cancer Epidemiology Biomarkers & Prevention.

[21]  Peter J. Woolf,et al.  GAGE: generally applicable gene set enrichment for pathway analysis , 2009, BMC Bioinformatics.

[22]  B. Pedersen,et al.  Exercise as a Mean to Control Low-Grade Systemic Inflammation , 2009, Mediators of inflammation.

[23]  R. Durazo-Arvizu,et al.  Effect of mindfulness based stress reduction on immune function, quality of life and coping in women newly diagnosed with early stage breast cancer , 2008, Brain, Behavior, and Immunity.

[24]  E. Winer,et al.  Impact of a mixed strength and endurance exercise intervention on insulin levels in breast cancer survivors. , 2008, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[25]  Daniela Fetter Telles Nunes,et al.  Relaxation and guided imagery program in patients with breast cancer undergoing radiotherapy is not associated with neuroimmunomodulatory effects. , 2007, Journal of psychosomatic research.

[26]  L. Carlson,et al.  One year pre–post intervention follow-up of psychological, immune, endocrine and blood pressure outcomes of mindfulness-based stress reduction (MBSR) in breast and prostate cancer outpatients , 2007, Brain, Behavior, and Immunity.

[27]  A. Ashworth,et al.  Molecular response to aromatase inhibitor treatment in primary breast cancer , 2007, Breast Cancer Research.

[28]  Roger B. Davis,et al.  A pilot study for a randomized, controlled trial on the effect of guided imagery in hospitalized medical patients. , 2007, Journal of alternative and complementary medicine.

[29]  K. Courneya,et al.  Randomized controlled trial of exercise and blood immune function in postmenopausal breast cancer survivors. , 2005, Journal of applied physiology.

[30]  H. Thompson Effects of physical activity and exercise on experimentally-induced mammary carcinogenesis , 1997, Breast Cancer Research and Treatment.

[31]  M. Dowsett,et al.  Effect of raloxifene on breast cancer cell Ki67 and apoptosis: a double-blind, placebo-controlled, randomized clinical trial in postmenopausal patients. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[32]  C. Ulrich,et al.  Anthropometric and hormone effects of an eight-week exercise-diet intervention in breast cancer patients: results of a pilot study. , 1998, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[33]  B E Ainsworth,et al.  A simultaneous evaluation of 10 commonly used physical activity questionnaires. , 1993, Medicine and science in sports and exercise.

[34]  R. Dishman,et al.  Reliability and concurrent validity for a 7-d re-call of physical activity in college students. , 1988, Medicine and science in sports and exercise.

[35]  K. Vranizan,et al.  Assessment of habitual physical activity by a seven-day recall in a community survey and controlled experiments. , 1985, American journal of epidemiology.

[36]  W L Haskell,et al.  Seven-day activity and self-report compared to a direct measure of physical activity. , 1984, American journal of epidemiology.