Breast Cancer Research and Treatment

, Volume 123, Issue 2, pp 531–542 | Cite as

Past recreational physical activity, body size, and all-cause mortality following breast cancer diagnosis: results from the breast cancer family registry

  • Theresa H. M. KeeganEmail author
  • Roger L. Milne
  • Irene L. Andrulis
  • Ellen T. Chang
  • Meera Sangaramoorthy
  • Kelly-Anne Phillips
  • Graham G. Giles
  • Pamela J. Goodwin
  • Carmel Apicella
  • John L. Hopper
  • Alice S. Whittemore
  • Esther M. John


Few studies have considered the joint association of body mass index (BMI) and physical activity, two modifiable factors, with all-cause mortality after breast cancer diagnosis. Women diagnosed with invasive breast cancer (n = 4,153) between 1991 and 2000 were enrolled in the Breast Cancer Family Registry through population-based sampling in Northern California, USA; Ontario, Canada; and Melbourne and Sydney, Australia. During a median follow-up of 7.8 years, 725 deaths occurred. Baseline questionnaires assessed moderate and vigorous recreational physical activity and BMI prior to diagnosis. Associations with all-cause mortality were assessed using Cox proportional hazards regression, adjusting for established prognostic factors. Compared with no physical activity, any recreational activity during the 3 years prior to diagnosis was associated with a 34% lower risk of death [hazard ratio (HR) = 0.66, 95% confidence interval (CI): 0.51–0.85] for women with estrogen receptor (ER)-positive tumors, but not those with ER-negative tumors; this association did not appear to differ by race/ethnicity or BMI. Lifetime physical activity was not associated with all-cause mortality. BMI was positively associated with all-cause mortality for women diagnosed at age ≥50 years with ER-positive tumors (compared with normal-weight women, HR for overweight = 1.39, 95% CI: 0.90–2.15; HR for obese = 1.77, 95% CI: 1.11–2.82). BMI associations did not appear to differ by race/ethnicity. Our findings suggest that physical activity and BMI exert independent effects on overall mortality after breast cancer.


Breast cancer Physical activity Body mass index Obesity Mortality 



The authors thank Enid Satariano and Jocelyn Koo (Northern California Cancer Center), Elaine Maloney and Nayana Weerasooriya (Cancer Care Ontario), and Maggie Angelakos, Judi Maskiell and Gillian Dite (University of Melbourne) for their assistance. The Breast Cancer Family Registry (Breast CFR) was supported by the National Cancer Institute, National Institutes of Health under RFA CA-95-011 and CA-06-503, and through cooperative agreements with members of the Breast CFR and Principal Investigators. The three registries contributing data to this analysis were supported by U01 CA69417 (Northern California Cancer Center), U01 CA69467 (Cancer Care Ontario), and U01 CA69638 (University of Melbourne). Kelly-Anne Phillips was supported by the Cancer Council Victoria Colebatch Clinical Research Fellowship. The content of this manuscript does not necessarily reflect the views or policies of the National Cancer Institute or any of the collaborating centers in the Breast CFR, nor does mention of trade names, commercial products, or organizations imply endorsement by the US Government or the Breast CFR.


  1. 1.
    Stewart BW, Kleihues P (2003) World cancer report. International agency for research on cancer. IARC Press, LyonGoogle Scholar
  2. 2.
    Sunga AY, Eberl MM, Oeffinger KC, Hudson MM, Mahoney MC (2005) Care of cancer survivors. Am Fam Physician 71:699–706PubMedGoogle Scholar
  3. 3.
    Stein KD, Syrjala KL, Andrykowski MA (2008) Physical and psychological long-term and late effects of cancer. Cancer 112:2577–2592CrossRefPubMedGoogle Scholar
  4. 4.
    Geiger AM, Thwin SS, Lash TL, Buist DS, Prout MN, Wei F, Field TS, Ulcickas Yood M, Frost FJ, Enger SM, Silliman RA (2007) Recurrences and second primary breast cancers in older women with initial early-stage disease. Cancer 109:966–974CrossRefPubMedGoogle Scholar
  5. 5.
    Carmichael AR (2006) Obesity as a risk factor for development and poor prognosis of breast cancer. Bjog 113:1160–1166PubMedGoogle Scholar
  6. 6.
    Chlebowski RT, Aiello E, McTiernan A (2002) Weight loss in breast cancer patient management. J Clin Oncol 20:1128–1143CrossRefPubMedGoogle Scholar
  7. 7.
    Rock CL, Demark-Wahnefried W (2002) Nutrition and survival after the diagnosis of breast cancer: a review of the evidence. J Clin Oncol 20:3302–3316CrossRefPubMedGoogle Scholar
  8. 8.
    Carmichael AR (2006) Obesity and prognosis of breast cancer. Obes Rev 7:333–340CrossRefPubMedGoogle Scholar
  9. 9.
    Loi S, Milne RL, Friedlander ML, McCredie MR, Giles GG, Hopper JL, Phillips KA (2005) Obesity and outcomes in premenopausal and postmenopausal breast cancer. Cancer Epidemiol Biomarkers Prev 14:1686–1691CrossRefPubMedGoogle Scholar
  10. 10.
    Holmes MD, Chen WY, Feskanich D, Kroenke CH, Colditz GA (2005) Physical activity and survival after breast cancer diagnosis. JAMA 293:2479–2486CrossRefPubMedGoogle Scholar
  11. 11.
    Abrahamson PE, Gammon MD, Lund MJ, Britton JA, Marshall SW, Flagg EW, Porter PL, Brinton LA, Eley JW, Coates RJ (2006) Recreational physical activity and survival among young women with breast cancer. Cancer 107:1777–1785CrossRefPubMedGoogle Scholar
  12. 12.
    Holick CN, Newcomb PA, Trentham-Dietz A, Titus-Ernstoff L, Bersch AJ, Stampfer MJ, Baron JA, Egan KM, Willett WC (2008) Physical activity and survival after diagnosis of invasive breast cancer. Cancer Epidemiol Biomarkers Prev 17:379–386CrossRefPubMedGoogle Scholar
  13. 13.
    Pierce JP, Stefanick ML, Flatt SW, Natarajan L, Sternfeld B, Madlensky L, Al-Delaimy WK, Thomson CA, Kealey S, Hajek R, Parker BA, Newman VA, Caan B, Rock CL (2007) Greater survival after breast cancer in physically active women with high vegetable-fruit intake regardless of obesity. J Clin Oncol 25:2345–2351CrossRefPubMedGoogle Scholar
  14. 14.
    Sternfeld B, Weltzien E, Quesenberry CP Jr, Castillo AL, Kwan M, Slattery ML, Caan BJ (2009) Physical activity and risk of recurrence and mortality in breast cancer survivors: findings from the LACE study. Cancer Epidemiol Biomarkers Prev 18:87–95CrossRefPubMedGoogle Scholar
  15. 15.
    Irwin ML, Smith AW, McTiernan A, Ballard-Barbash R, Cronin K, Gilliland FD, Baumgartner RN, Baumgartner KB, Bernstein L (2008) Influence of pre- and postdiagnosis physical activity on mortality in breast cancer survivors: the health, eating, activity, and lifestyle study. J Clin Oncol 26:3958–3964CrossRefPubMedGoogle Scholar
  16. 16.
    West-Wright CN, Henderson KD, Sullivan-Halley J, Ursin G, Deapen D, Neuhausen S, Reynolds P, Chang E, Ma H, Bernstein L (2009) Long-term and recent recreational physical activity and survival after breast cancer: the California Teachers Study. Cancer Epidemiol Biomarkers Prev 18:2851–2859CrossRefPubMedGoogle Scholar
  17. 17.
    Borugian MJ, Sheps SB, Kim-Sing C, Van Patten C, Potter JD, Dunn B, Gallagher RP, Hislop TG (2004) Insulin, macronutrient intake, and physical activity: are potential indicators of insulin resistance associated with mortality from breast cancer? Cancer Epidemiol Biomarkers Prev 13:1163–1172PubMedGoogle Scholar
  18. 18.
    Enger SM, Bernstein L (2004) Exercise activity, body size and premenopausal breast cancer survival. Br J Cancer 90:2138–2141PubMedGoogle Scholar
  19. 19.
    Rohan TE, Fu W, Hiller JE (1995) Physical activity and survival from breast cancer. Eur J Cancer Prev 4:419–424CrossRefPubMedGoogle Scholar
  20. 20.
    John EM, Hopper JL, Beck JC, Knight JA, Neuhausen SL, Senie RT, Ziogas A, Andrulis IL, Anton-Culver H, Boyd N, Buys SS, Daly MB, O’Malley FP, Santella RM, Southey MC, Venne VL, Venter DJ, West DW, Whittemore AS, Seminara D (2004) The Breast Cancer Family Registry: an infrastructure for cooperative multinational, interdisciplinary and translational studies of the genetic epidemiology of breast cancer. Breast Cancer Res 6:R375–R389CrossRefPubMedGoogle Scholar
  21. 21.
    Chang ET, Milne RL, Phillips KA, Figueiredo JC, Sangaramoorthy M, Keegan TH, Andrulis IL, Hopper JL, Goodwin PJ, O’Malley FP, Weerasooriya N, Apicella C, Southey MC, Friedlander ML, Giles GG, Whittemore AS, West DW, John EM (2009) Family history of breast cancer and all-cause mortality after breast cancer diagnosis in the Breast Cancer Family Registry. Breast Cancer Res Treat 117:167–176CrossRefPubMedGoogle Scholar
  22. 22.
    Bianchini F, Kaaks R, Vainio H (2002) Overweight, obesity, and cancer risk. Lancet Oncol 3:565–574CrossRefPubMedGoogle Scholar
  23. 23.
    Ainsworth BE, Haskell WL, Whitt MC, Irwin ML, Swartz AM, Strath SJ, O’Brien WL, Bassett DR Jr, Schmitz KH, Emplaincourt PO, Jacobs DR Jr, Leon AS (2000) Compendium of physical activities: an update of activity codes and MET intensities. Med Sci Sports Exerc 32:S498–S504CrossRefPubMedGoogle Scholar
  24. 24.
    Phillips KA, Milne RL, West DW, Goodwin PJ, Giles GG, Chang ET, Figueiredo JC, Friedlander ML, Keegan TH, Glendon G, Apicella C, O’Malley FP, Southey MC, Andrulis IL, John EM, Hopper JL (2009) Prediagnosis reproductive factors and all-cause mortality for women with breast cancer in the breast cancer family registry. Cancer Epidemiol Biomarkers Prev 18:1792–1797CrossRefPubMedGoogle Scholar
  25. 25.
    Dal Maso L, Zucchetto A, Talamini R, Serraino D, Stocco CF, Vercelli M, Falcini F, Franceschi S (2008) Effect of obesity and other lifestyle factors on mortality in women with breast cancer. Int J Cancer 123:2188–2194CrossRefPubMedGoogle Scholar
  26. 26.
    Tao MH, Shu XO, Ruan ZX, Gao YT, Zheng W (2006) Association of overweight with breast cancer survival. Am J Epidemiol 163:101–107CrossRefPubMedGoogle Scholar
  27. 27.
    Barnett GC, Shah M, Redman K, Easton DF, Ponder BA, Pharoah PD (2008) Risk factors for the incidence of breast cancer: do they affect survival from the disease? J Clin Oncol 26:3310–3316CrossRefPubMedGoogle Scholar
  28. 28.
    Maehle BO, Tretli S (1996) Pre-morbid body-mass-index in breast cancer: reversed effect on survival in hormone receptor negative patients. Breast Cancer Res Treat 41:123–130CrossRefPubMedGoogle Scholar
  29. 29.
    Majed B, Moreau T, Senouci K, Salmon RJ, Fourquet A, Asselain B (2008) Is obesity an independent prognosis factor in woman breast cancer? Breast Cancer Res Treat 111:329–342CrossRefPubMedGoogle Scholar
  30. 30.
    Daling JR, Malone KE, Doody DR, Johnson LG, Gralow JR, Porter PL (2001) Relation of body mass index to tumor markers and survival among young women with invasive ductal breast carcinoma. Cancer 92:720–729CrossRefPubMedGoogle Scholar
  31. 31.
    Whiteman MK, Hillis SD, Curtis KM, McDonald JA, Wingo PA, Marchbanks PA (2005) Body mass and mortality after breast cancer diagnosis. Cancer Epidemiol Biomarkers Prev 14:2009–2014CrossRefPubMedGoogle Scholar
  32. 32.
    Abrahamson PE, Gammon MD, Lund MJ, Flagg EW, Porter PL, Stevens J, Swanson CA, Brinton LA, Eley JW, Coates RJ (2006) General and abdominal obesity and survival among young women with breast cancer. Cancer Epidemiol Biomarkers Prev 15:1871–1877CrossRefPubMedGoogle Scholar
  33. 33.
    Berclaz G, Li S, Price KN, Coates AS, Castiglione-Gertsch M, Rudenstam CM, Holmberg SB, Lindtner J, Erien D, Collins J, Snyder R, Thurlimann B, Fey MF, Mendiola C, Werner ID, Simoncini E, Crivellari D, Gelber RD, Goldhirsch A (2004) Body mass index as a prognostic feature in operable breast cancer: the International Breast Cancer Study Group experience. Ann Oncol 15:875–884CrossRefPubMedGoogle Scholar
  34. 34.
    Ligibel JA, Campbell N, Partridge A, Chen WY, Salinardi T, Chen H, Adloff K, Keshaviah A, Winer EP (2008) Impact of a mixed strength and endurance exercise intervention on insulin levels in breast cancer survivors. J Clin Oncol 26:907–912CrossRefPubMedGoogle Scholar
  35. 35.
    Bianchini F, Kaaks R, Vainio H (2002) Weight control and physical activity in cancer prevention. Obes Rev 3:5–8CrossRefPubMedGoogle Scholar
  36. 36.
    Goodwin PJ, Ennis M, Pritchard KI, Trudeau ME, Koo J, Madarnas Y, Hartwick W, Hoffman B, Hood N (2002) Fasting insulin and outcome in early-stage breast cancer: results of a prospective cohort study. J Clin Oncol 20:42–51CrossRefPubMedGoogle Scholar
  37. 37.
    Goodwin PJ, Ennis M, Pritchard KI, Trudeau ME, Koo J, Hartwick W, Hoffma B, Hood N (2002) Insulin-like growth factor binding proteins 1 and 3 and breast cancer outcomes. Breast Cancer Res Treat 74:65–76CrossRefPubMedGoogle Scholar
  38. 38.
    Del Giudice ME, Fantus IG, Ezzat S, McKeown-Eyssen G, Page D, Goodwin PJ (1998) Insulin and related factors in premenopausal breast cancer risk. Breast Cancer Res Treat 47:111–120CrossRefPubMedGoogle Scholar
  39. 39.
    Suga K, Imai K, Eguchi H, Hayashi S, Higashi Y, Nakachi K (2001) Molecular significance of excess body weight in postmenopausal breast cancer patients, in relation to expression of insulin-like growth factor I receptor and insulin-like growth factor II genes. Jpn J Cancer Res 92:127–134PubMedGoogle Scholar
  40. 40.
    John EM, Horn-Ross PL, Koo J (2003) Lifetime physical activity and breast cancer risk in a multiethnic population: the San Francisco Bay area breast cancer study. Cancer Epidemiol Biomarkers Prev 12:1143–1152PubMedGoogle Scholar
  41. 41.
    Rhodes RE, Courneya KS, Bobick TM (2001) Personality and exercise participation across the breast cancer experience. Psychooncology 10:380–388CrossRefPubMedGoogle Scholar
  42. 42.
    Courneya KS, Friedenreich CM (1997) Relationship between exercise during treatment and current quality of life among survivors of breast cancer. J Psychoso Oncol 15:35–57CrossRefGoogle Scholar
  43. 43.
    Bernstein L, Henderson BE, Hanisch R, Sullivan-Halley J, Ross RK (1994) Physical exercise and reduced risk of breast cancer in young women. J Natl Cancer Inst 86:1403–1408CrossRefPubMedGoogle Scholar
  44. 44.
    Chasan-Taber L, Erickson JB, McBride JW, Nasca PC, Chasan-Taber S, Freedson PS (2002) Reproducibility of a self-administered lifetime physical activity questionnaire among female college alumnae. Am J Epidemiol 155:282–289CrossRefPubMedGoogle Scholar
  45. 45.
    Kriska AM, Knowler WC, LaPorte RE, Drash AL, Wing RR, Blair SN, Bennett PH, Kuller LH (1990) Development of questionnaire to examine relationship of physical activity and diabetes in Pima Indians. Diabetes Care 13:401–411CrossRefPubMedGoogle Scholar
  46. 46.
    Kriska AM, Sandler RB, Cauley JA, LaPorte RE, Hom DL, Pambianco G (1988) The assessment of historical physical activity and its relation to adult bone parameters. Am J Epidemiol 127:1053–1063PubMedGoogle Scholar
  47. 47.
    Satariano WA (1993) Aging, comorbidity, and breast cancer survival: an epidemiologic view. Adv Exp Med Biol 330:1–11PubMedGoogle Scholar
  48. 48.
    Satariano WA, Ragland DR (1994) The effect of comorbidity on 3-year survival of women with primary breast cancer. Ann Intern Med 120:104–110PubMedGoogle Scholar
  49. 49.
    Tammemagi CM, Nerenz D, Neslund-Dudas C, Feldkamp C, Nathanson D (2005) Comorbidity and survival disparities among black and white patients with breast cancer. JAMA 294:1765–1772CrossRefPubMedGoogle Scholar
  50. 50.
    Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ (2003) Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 348:1625–1638CrossRefPubMedGoogle Scholar
  51. 51.
    Ezzati M, Martin H, Skjold S, Vander Hoorn S, Murray CJ (2006) Trends in national and state-level obesity in the USA after correction for self-report bias: analysis of health surveys. J R Soc Med 99:250–257CrossRefPubMedGoogle Scholar
  52. 52.
    Villanueva EV (2001) The validity of self-reported weight in US adults: a population based cross-sectional study. BMC Public Health 1:11CrossRefPubMedGoogle Scholar
  53. 53.
    Spencer EA, Appleby PN, Davey GK, Key TJ (2002) Validity of self-reported height and weight in 4808 EPIC-Oxford participants. Public Health Nutr 5:561–565CrossRefPubMedGoogle Scholar
  54. 54.
    Friedenreich CM, Cust AE (2008) Physical activity and breast cancer risk: impact of timing, type and dose of activity and population subgroup effects. Br J Sports Med 42:636–647CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC. 2010

Authors and Affiliations

  • Theresa H. M. Keegan
    • 1
    • 2
    Email author
  • Roger L. Milne
    • 3
    • 4
  • Irene L. Andrulis
    • 5
    • 6
  • Ellen T. Chang
    • 1
    • 2
  • Meera Sangaramoorthy
    • 1
  • Kelly-Anne Phillips
    • 7
    • 8
  • Graham G. Giles
    • 9
  • Pamela J. Goodwin
    • 5
    • 10
  • Carmel Apicella
    • 4
  • John L. Hopper
    • 4
  • Alice S. Whittemore
    • 2
  • Esther M. John
    • 1
    • 2
  1. 1.Northern California Cancer CenterFremontUSA
  2. 2.Division of Epidemiology, Department of Health Research and PolicyStanford University School of MedicineStanfordUSA
  3. 3.Genetic & Molecular Epidemiology Group, Human Cancer Genetics ProgramSpanish National Cancer Center (CNIO)MadridSpain
  4. 4.Centre for Molecular, Environmental, Genetic and Analytic Epidemiology, School of Population HealthThe University of MelbourneMelbourneAustralia
  5. 5.Samuel Lunenfeld Research Institute, Mount Sinai HospitalUniversity of TorontoTorontoCanada
  6. 6.Ontario Cancer Genetics NetworkCancer Care OntarioTorontoCanada
  7. 7.Division of Haematology and Medical OncologyPeter MacCallum Cancer CentreMelbourneAustralia
  8. 8.Department of Medicine, St. Vincent’s HospitalThe University of MelbourneMelbourneAustralia
  9. 9.Cancer Epidemiology CentreThe Cancer Council VictoriaCarltonAustralia
  10. 10.Departments of Medicine and Public Health Sciences, Faculty of MedicineUniversity of TorontoTorontoCanada

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