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Trajectories of objectively measured physical function among older breast cancer survivors in comparison with cancer-free controls

  • Epidemiology
  • Published:
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Abstract

Purpose

Aging associated with progressive declines in physical function is well-known; however, it is unclear how breast cancer diagnosis affects the trajectories of physical function over a long period of time. The current study examined the trajectories in objective measures of physical function over 20 years for women with breast cancer and matched controls.

Methods

2712 community-dwelling women (452 breast cancer cases and 1:5 matched cancer-free controls) aged 65 years or older at baseline (1986–1988) within the Study of Osteoporotic Fractures were followed for 20 years. Objective physical function was assessed up to 9 times, including hand grip strength, timed chair stand, gait speed and quadriceps strength. Linear mixed models were used to model physical function changes in terms of secular time trend, group (cases or controls), period (pre-and post-diagnosis status), and their interaction terms.

Results

We observed all measures of physical function declined over time. While no differences in trends between cases and controls during the pre-diagnosis period were observed, after cancer diagnosis, grip strength and gait speed declined significantly faster in cases than controls. Quadriceps strength significantly decreased ~ 7 pounds shortly after breast cancer diagnosis, and then improved over time.

Conclusion

Our study revealed that older breast cancer survivors relative to older women without cancer had significantly worse declines in grip strength and gait speed. Breast cancer survivors also had a sharp, short-term drop followed by gradual improvement over time in quadriceps strength. These findings suggest exercise training targeting muscle strength and mobility would be beneficial among older breast cancer survivors.

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Data availability

The data are available from the National Institute on Aging (NIA) AgingResearchBiobank upon reasonable request (https://agingresearchbiobank.nia.nih.gov/).

Code availability

Not applicable.

References

  1. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F (2021) Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin 71:209–249. https://doi.org/10.3322/caac.21660

    Article  PubMed  Google Scholar 

  2. ASC (2020) Survival Rates for Breast Cancer. https://www.cancer.org/cancer/breast-cancer/understanding-a-breast-cancer-diagnosis/breast-cancer-survival-rates.html. In: American Cancer Society (ASC)

  3. Jordan JH, Thwin SS, Lash TL, Buist DS, Field TS, Haque R, Pawloski PA, Petersen HV, Prout MN, Quinn VP, Yood MU, Silliman RA, Geiger AM (2014) Incident comorbidities and all-cause mortality among 5-year survivors of Stage I and II breast cancer diagnosed at age 65 or older: a prospective-matched cohort study. Breast Cancer Res Treat 146:401–409. https://doi.org/10.1007/s10549-014-3021-8

    Article  PubMed  PubMed Central  Google Scholar 

  4. Chang L, Weiner LS, Hartman SJ, Horvath S, Jeste D, Mischel PS, Kado DM (2019) Breast cancer treatment and its effects on aging. J Geriatr Oncol 10:346–355. https://doi.org/10.1016/j.jgo.2018.07.010

    Article  PubMed  Google Scholar 

  5. Magnuson A, Lei L, Gilmore N, Kleckner AS, Lin FV, Ferguson R, Hurria A, Wittink MN, Esparaz BT, Giguere JK, Misleh J, Bautista J, Mohile SG, Janelsins MC (2019) Longitudinal relationship between frailty and cognition in patients 50 years and older with breast cancer. J Am Geriatr Soc 67:928–936. https://doi.org/10.1111/jgs.15934

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ahles TA, Root JC, Ryan EL (2012) Cancer- and cancer treatment-associated cognitive change: an update on the state of the science. J Clin Oncol 30:3675–3686. https://doi.org/10.1200/JCO.2012.43.0116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Hodgson KD, Hutchinson AD, Wilson CJ, Nettelbeck T (2013) A meta-analysis of the effects of chemotherapy on cognition in patients with cancer. Cancer Treat Rev 39:297–304. https://doi.org/10.1016/j.ctrv.2012.11.001

    Article  CAS  PubMed  Google Scholar 

  8. Jim HS, Phillips KM, Chait S, Faul LA, Popa MA, Lee YH, Hussin MG, Jacobsen PB, Small BJ (2012) Meta-analysis of cognitive functioning in breast cancer survivors previously treated with standard-dose chemotherapy. J Clin Oncol 30:3578–3587. https://doi.org/10.1200/JCO.2011.39.5640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Kroenke CH, Rosner B, Chen WY, Kawachi I, Colditz GA, Holmes MD (2004) Functional impact of breast cancer by age at diagnosis. J Clin Oncol 22:1849–1856. https://doi.org/10.1200/Jco.2004.04.173

    Article  PubMed  Google Scholar 

  10. Michael YL, Kawachi I, Berkman LF, Holmes MD, Colditz GA (2000) The persistent impact of breast carcinoma on functional health status: prospective evidence from the Nurses’ Health Study. Cancer 89:2176–2186. https://doi.org/10.1002/1097-0142(20001201)89:11%3c2176::aid-cncr5%3e3.0.co;2-6

    Article  CAS  PubMed  Google Scholar 

  11. Karlsen RV, Frederiksen K, Larsen MB, von Heymann-Horan AB, Appel CW, Christensen J, Tjonneland A, Ross L, Johansen C, Bidstrup PE (2016) The impact of a breast cancer diagnosis on health-related quality of life. A prospective comparison among middle-aged to elderly women with and without breast cancer. Acta Oncol 55:720–727. https://doi.org/10.3109/0284186X.2015.1127415

    Article  PubMed  Google Scholar 

  12. Michael YL, Wu C, Pan K, Seguin-Fowler RA, Garcia DO, Zaslavsky O, Chlebowski RT (2020) Postmenopausal breast cancer and physical function change: a difference-in-differences analysis. J Am Geriatr Soc 68:1029–1036. https://doi.org/10.1111/jgs.16323

    Article  PubMed  Google Scholar 

  13. Hsu T, Ennis M, Hood N, Graham M, Goodwin PJ (2013) Quality of life in long-term breast cancer survivors. J Clin Oncol 31:3540–3548. https://doi.org/10.1200/JCO.2012.48.1903

    Article  PubMed  Google Scholar 

  14. Peuckmann V, Ekholm O, Rasmussen NK, Moller S, Groenvold M, Christiansen P, Eriksen J, Sjogren P (2007) Health-related quality of life in long-term breast cancer survivors: nationwide survey in Denmark. Breast Cancer Res Treat 104:39–46. https://doi.org/10.1007/s10549-006-9386-6

    Article  PubMed  Google Scholar 

  15. Klein D, Mercier M, Abeilard E, Puyraveau M, Danzon A, Dalstein V, Pozet A, Guizard AV, Henry-Amar M, Velten M (2011) Long-term quality of life after breast cancer: a French registry-based controlled study. Breast Cancer Res Treat 129:125–134. https://doi.org/10.1007/s10549-011-1408-3

    Article  PubMed  Google Scholar 

  16. Winters-Stone KM, Medysky ME, Savin MA (2019) Patient-reported and objectively measured physical function in older breast cancer survivors and cancer-free controls. J Geriatr Oncol 10:311–316. https://doi.org/10.1016/j.jgo.2018.10.006

    Article  PubMed  Google Scholar 

  17. Williams GR, Chen Y, Kenzik KM, McDonald A, Shachar SS, Klepin HD, Kritchevsky S, Bhatia S (2020) Assessment of sarcopenia measures, survival, and disability in older adults before and after diagnosis with cancer. JAMA Netw Open 3:e204783. https://doi.org/10.1001/jamanetworkopen.2020.4783

    Article  PubMed  PubMed Central  Google Scholar 

  18. Guida JL, Ahles TA, Belsky D, Campisi J, Cohen HJ, DeGregori J, Fuldner R, Ferrucci L, Gallicchio L, Gavrilov L, Gavrilova N, Green PA, Jhappan C, Kohanski R, Krull K, Mandelblatt J, Ness KK, O’Mara A, Price N, Schrack J, Studenski S, Theou O, Tracy RP, Hurria A (2019) Measuring aging and identifying aging phenotypes in cancer survivors. J Natl Cancer Inst 111:1245–1254. https://doi.org/10.1093/jnci/djz136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Zhu J, Wang F, Shi L, Cai H, Zheng Y, Zheng W, Bao P, Shu XO (2020) Accelerated aging in breast cancer survivors and its association with mortality and cancer recurrence. Breast Cancer Res Treat 180:449–459. https://doi.org/10.1007/s10549-020-05541-5

    Article  PubMed  PubMed Central  Google Scholar 

  20. Cummings SR, Black DM, Nevitt MC, Browner WS, Cauley JA, Genant HK, Mascioli SR, Scott JC, Seeley DG, Steiger P et al (1990) Appendicular bone density and age predict hip fracture in women. The Study of Osteoporotic Fractures Research Group. JAMA 263:665–668

    Article  CAS  Google Scholar 

  21. Grandits G, Neuhaus J (2010) Using SAS® to Perform Individual Matching in Design of Case-Control Studies https://support.sas.com/resources/papers/proceedings10/061-2010.pdf. In: SAS Global Forum

  22. Jakobsen LH, Rask IK, Kondrup J (2010) Validation of handgrip strength and endurance as a measure of physical function and quality of life in healthy subjects and patients. Nutrition 26:542–550. https://doi.org/10.1016/j.nut.2009.06.015

    Article  PubMed  Google Scholar 

  23. Bohannon RW (2008) Hand-grip dynamometry predicts future outcomes in aging adults. J Geriatr Phys Ther 31:3–10. https://doi.org/10.1519/00139143-200831010-00002

    Article  PubMed  Google Scholar 

  24. Penninx BWJH, Ferrucci L, Leveille SG, Rantanen T, Pahor M, Guralnik JM (2000) Lower extremity performance in nondisabled older persons as a predictor of subsequent hospitalization. J Gerontol a-Biol 55:M691–M697. https://doi.org/10.1093/gerona/55.11.M691

    Article  CAS  Google Scholar 

  25. Guralnik JM, Simonsick EM, Ferrucci L, Glynn RJ, Berkman LF, Blazer DG, Scherr PA, Wallace RB (1994) A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission. J Gerontol 49:M85-94. https://doi.org/10.1093/geronj/49.2.m85

    Article  CAS  PubMed  Google Scholar 

  26. Heidari B (2011) Knee osteoarthritis prevalence, risk factors, pathogenesis and features: part I. Caspian J Intern Med 2:205–212

    PubMed  PubMed Central  Google Scholar 

  27. Ito Y, Aoki T, Sato T, Oishi K, Ishii K (2020) Comparison of quadriceps setting strength and knee extension strength tests to evaluate lower limb muscle strength based on health-related physical fitness values in elderly people. Bmj Open Sport Exerc. https://doi.org/10.1136/bmjsem-2020-000753

    Article  Google Scholar 

  28. Warton EM (2020) Time after time: difference-in-differences and interrupted time series models in SAS. In: SAS Global Forum 2020

  29. Carter SJ, Hunter GR, Norian LA, Turan B, Rogers LQ (2018) Ease of walking associates with greater free-living physical activity and reduced depressive symptomology in breast cancer survivors: pilot randomized trial. Support Care Cancer 26:1675–1683. https://doi.org/10.1007/s00520-017-4015-y

    Article  PubMed  Google Scholar 

  30. Rogers LQ, Courneya KS, Carter SJ, Anton PM, Verhulst S, Vicari SK, Robbs RS, McAuley E (2016) Effects of a multicomponent physical activity behavior change intervention on breast cancer survivor health status outcomes in a randomized controlled trial. Breast Cancer Res Treat 159:283–291. https://doi.org/10.1007/s10549-016-3945-2

    Article  PubMed  PubMed Central  Google Scholar 

  31. Winters-Stone KM, Horak F, Jacobs PG, Trubowitz P, Dieckmann NF, Stoyles S, Faithfull S (2017) Falls, functioning, and disability among women with persistent symptoms of chemotherapy-induced peripheral neuropathy. J Clin Oncol 35:2604. https://doi.org/10.1200/Jco.2016.71.3552

    Article  PubMed  PubMed Central  Google Scholar 

  32. Sweeney C, Schmitz KH, Lazovich D, Virnig BA, Wallace RB, Folsom AR (2006) Functional limitations in elderly female cancer survivors. J Natl Cancer Inst 98:521–529. https://doi.org/10.1093/jnci/djj130

    Article  PubMed  Google Scholar 

  33. Avis NE, Deimling GT (2008) Cancer survivorship and aging. Cancer 113:3519–3529. https://doi.org/10.1002/cncr.23941

    Article  PubMed  Google Scholar 

  34. Hurria A, Soto-Perez-de-Celis E, Allred JB, Cohen HJ, Arsenyan A, Ballman K, Le-Rademacher J, Jatoi A, Filo J, Mandelblatt J, Lafky JM, Kimmick G, Klepin HD, Freedman RA, Burstein H, Gralow J, Wolff AC, Magrinat G, Barginear M, Muss H (2019) Functional decline and resilience in older women receiving adjuvant chemotherapy for breast cancer. J Am Geriatr Soc 67:920–927. https://doi.org/10.1111/jgs.15493

    Article  PubMed  Google Scholar 

  35. Iwakura M, Okura K, Kubota M, Sugawara K, Kawagoshi A, Takahashi H, Shioya T (2021) Estimation of minimal clinically important difference for quadriceps and inspiratory muscle strength in older outpatients with chronic obstructive pulmonary disease: a prospective cohort study. Phys Ther Res 24:35–42. https://doi.org/10.1298/ptr.E10049

    Article  PubMed  Google Scholar 

  36. Euhus DM, Addae JK, Snyder CF, Canner JK (2019) Change in health-related quality of life in older women after diagnosis of a small breast cancer. Cancer 125:1807–1814. https://doi.org/10.1002/cncr.31993

    Article  CAS  PubMed  Google Scholar 

  37. Cohen HJ, Lan L, Archer L, Kornblith AB (2012) Impact of age, comorbidity and symptoms on physical function in long-term breast cancer survivors (CALGB 70803). J Geriatr Oncol 3:82–89. https://doi.org/10.1016/j.jgo.2012.01.005

    Article  PubMed  PubMed Central  Google Scholar 

  38. Lazovich D, Robien K, Cutler G, Virnig B, Sweeney C (2009) Quality of life in a prospective cohort of elderly women with and without cancer. Cancer 115:4283–4297. https://doi.org/10.1002/cncr.24580

    Article  PubMed  Google Scholar 

  39. Satariano WA, Ragland DR (1996) Upper-body strength and breast cancer: a comparison of the effects of age and disease. J Gerontol A Biol Sci Med Sci 51:M215-219. https://doi.org/10.1093/gerona/51a.5.m215

    Article  CAS  PubMed  Google Scholar 

  40. Petrick JL, Reeve BB, Kucharska-Newton AM, Foraker RE, Platz EA, Stearns SC, Han XS, Windham BG, Irwin DE (2014) Functional status declines among cancer survivors: trajectory and contributing factors. J Geriatr Oncol 5:359–367. https://doi.org/10.1016/j.jgo.2014.06.002

    Article  PubMed  PubMed Central  Google Scholar 

  41. Peel NM, Kuys SS, Klein K (2013) Gait speed as a measure in geriatric assessment in clinical settings: a systematic review. J Gerontol a-Biol 68:39–46. https://doi.org/10.1093/gerona/gls174

    Article  Google Scholar 

  42. Studenski S, Perera S, Patel K, Rosano C, Faulkner K, Inzitari M, Brach J, Chandler J, Cawthon P, Connor EB, Nevitt M, Visser M, Kritchevsky S, Badinelli S, Harris T, Newman AB, Cauley J, Ferrucci L, Guralnik J (2011) Gait speed and survival in older adults. JAMA 305:50–58. https://doi.org/10.1001/jama.2010.1923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Yates T, Zaccardi F, Dhalwani NN, Davies MJ, Bakrania K, Celis-Morales CA, Gill JMR, Franks PW, Khunti K (2017) Association of walking pace and handgrip strength with all-cause, cardiovascular, and cancer mortality: a UK Biobank observational study. Eur Heart J 38:3232–3240. https://doi.org/10.1093/eurheartj/ehx449

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We would like to acknowledge the contribution of the Study of Osteoporotic Fractures (SOF) Investigators and the National Institute on Aging (NIA) AgingResearchBiobank (https://agingresearchbiobank.nia.nih.gov/) where the SOF collection of biospecimens and data is maintained.

Funding

Dr. Luo is partially supported by the National Institutes of Health (R03CA256238). Dr. Cespedes is partially supported by K01CA226155; R01AG065334; R01CA240394; R01CA251589. Dr. Carter receives support from the National Cancer Institute (R01CA235598) and the Indiana Clinical and Translational Sciences Institute (UL1TR002529).

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Authors and Affiliations

  1. Department of Epidemiology and Biostatistics, School of Public Health, Indiana University, Bloomington, IN, 47405, USA

    Juhua Luo

  2. Department of Kinesiology, School of Public Health, Indiana University, Bloomington, IN, USA

    Stephen J. Carter

  3. Indiana University Melvin and Bren Simon Comprehensive Cancer Center, Indianapolis, IS, 46202, USA

    Stephen J. Carter

  4. Division of Research, Kaiser Permanente Northern California, 2000 Broadway, Oakland, CA, 94612, USA

    Elizabeth M. Cespedes Feliciano

  5. Department of Environmental and Occupational Health, School of Public Health, Indiana University, Bloomington, IN, USA

    Michael Hendryx

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  1. Juhua Luo
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  3. Elizabeth M. Cespedes Feliciano
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  4. Michael Hendryx
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Contributions

JL contributed to the study concept and design, acquisition of data, data management, analysis and interpretation of data, and drafting of the manuscript. MH contributed to the study concept and design, interpretation of data, and critical review and revision of the manuscript. SJC and EMCF contributed to interpretation of data and critical review and revision of the manuscript. JL is the guarantor of this work and, as such, had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

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Correspondence to Juhua Luo.

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The authors declare no potential conflicts of interest.

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This is a secondary data analysis. In accordance with 45 CFR 46.101(b) and/or IU HRPP Policy, the study is granted exemption (category 4): Secondary research for which consent is not required.

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Luo, J., Carter, S.J., Feliciano, E.M.C. et al. Trajectories of objectively measured physical function among older breast cancer survivors in comparison with cancer-free controls. Breast Cancer Res Treat 193, 467–476 (2022). https://doi.org/10.1007/s10549-022-06568-6

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