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Effects of exercise on sleep problems in breast cancer patients receiving radiotherapy: a randomized clinical trial

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Breast Cancer Research and Treatment Aims and scope Submit manuscript

Abstract

Purpose

Sleep problems frequently affect breast cancer patients during and after treatment and reduce their quality of life. Treatment strategies are mostly unknown. Thus, we assessed within a randomized controlled trial whether a 12-week exercise program starting with the radiotherapy influences sleep trajectories.

Methods

Sleep quality and problems were assessed via self-report in 160 breast cancer patients before, during, and 2, 6, and 12 months after participation in a trial investigating resistance exercise versus a relaxation control group concomitant with radiotherapy. As additional comparison group, 25 age-matched healthy women exercised and followed identical study procedures. Ordinal logistic regression analyses were used.

Results

The exercise intervention significantly decreased sleep problems compared to the relaxation control group (scale: 0–100, with between-group mean differences of −10.2 (p = 0.03) from baseline to the end of radiotherapy and −10.9 (p = 0.005) to the end of the intervention), with sleep problems decreasing in the exercise group and increasing in the control group. At 12 months, differences were still observed but statistically non-significant (mean difference = −5.9, p = 0.20). Further adjustment for potential confounders did not change the results. Several determinants of sleep problems at baseline were identified, e.g., previous chemotherapy and higher body mass index.

Conclusions

Our randomized exercise intervention trial confirmed results from earlier but mostly smaller studies that radiotherapy aggravates sleep problems in breast cancer patients and that exercise can ameliorate these effects. Considering that sleep quality can be a major predictor of quality of life, our findings are of substantial importance to many breast cancer patients.

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Abbreviations

ANCOVA:

Analysis of covariance

BC :

Breast Cancer

BMI:

Body mass index

CES-D:

Center for epidemiological studies depression scale

FAQ:

Fatigue assessment questionnaire

MSPSS:

Multidimensional scale of perceived social support

OLR:

Ordinal logistic regression

References

  1. Savard J, Villa J, Ivers H, Simard S, Morin CM (2009) Prevalence, natural course, and risk factors of insomnia comorbid with cancer over a 2-month period. J Clin Oncol 27(31):5233–5239. doi:10.1200/JCO.2008.21.6333

    Article  PubMed  Google Scholar 

  2. Vargas S, Wohlgemuth WK, Antoni MH, Lechner SC, Holley HA, Carver CS (2010) Sleep dysfunction and psychosocial adaptation among women undergoing treatment for non-metastatic breast cancer. Psycho-oncology 19(6):669–673. doi:10.1002/pon.1603

    Article  PubMed  PubMed Central  Google Scholar 

  3. Liu L, Fiorentino L, Natarajan L, Parker BA, Mills PJ, Sadler GR, Dimsdale JE, Rissling M, He F, Ancoli-Israel S (2009) Pre-treatment symptom cluster in breast cancer patients is associated with worse sleep, fatigue and depression during chemotherapy. Psycho-Oncology 18(2):187–194

    Article  PubMed  PubMed Central  Google Scholar 

  4. Bower JE (2014) Cancer-related fatigue–mechanisms, risk factors, and treatments. Nature Rev Clin Oncol 11(10):597–609. doi:10.1038/nrclinonc.2014.127

    Article  CAS  Google Scholar 

  5. Van Onselen C, Paul SM, Lee K, Dunn L, Aouizerat BE, West C, Dodd M, Cooper B, Miaskowski C (2013) Trajectories of sleep disturbance and daytime sleepiness in women before and after surgery for breast cancer. J Pain Symptom Manag 45(2):244–260. doi:10.1016/j.jpainsymman.2012.02.020

    Article  Google Scholar 

  6. Savard J, Ivers H, Savard MH, Morin CM (2015) Cancer treatments and their side effects are associated with aggravation of insomnia: results of a longitudinal study. Cancer 121(10):1703–1711. doi:10.1002/cncr.29244

    Article  PubMed  Google Scholar 

  7. Costa AR, Fontes F, Pereira S, Goncalves M, Azevedo A, Lunet N (2014) Impact of breast cancer treatments on sleep disturbances—A systematic review. Breast 23(6):697–709. doi:10.1016/j.breast.2014.09.003

    Article  PubMed  Google Scholar 

  8. Palesh OG, Roscoe JA, Mustian KM, Roth T, Savard J, Ancoli-Israel S, Heckler C, Purnell JQ, Janelsins MC, Morrow GR (2010) Prevalence, demographics, and psychological associations of sleep disruption in patients with cancer: university of rochester cancer center-community clinical oncology program. J Clin Oncol 28(2):292–298. doi:10.1200/JCO.2009.22.5011

    Article  PubMed  Google Scholar 

  9. Liu L, Fiorentino L, Natarajan L, Parker BA, Mills PJ, Sadler GR, Dimsdale JE, Rissling M, He F, Ancoli-Israel S (2009) Pre-treatment symptom cluster in breast cancer patients is associated with worse sleep, fatigue and depression during chemotherapy. Psycho-Oncology 18(2):187–194. doi:10.1002/pon.1412

    Article  PubMed  PubMed Central  Google Scholar 

  10. Omne-Ponten M, Holmberg L, Burns T, Adami HO, Bergstrom R (1992) Determinants of the psycho-social outcome after operation for breast cancer. Results of a prospective comparative interview study following mastectomy and breast conservation. Eur J Cancer 28A(6–7):1062–1067

    Article  CAS  PubMed  Google Scholar 

  11. Chandwani KD, Perkins G, Nagendra HR, Raghuram NV, Spelman A, Nagarathna R, Johnson K, Fortier A, Arun B, Wei Q, Kirschbaum C, Haddad R, Morris GS, Scheetz J, Chaoul A, Cohen L (2014) Randomized, controlled trial of yoga in women with breast cancer undergoing radiotherapy. J Clin Oncol 32(10):1058–1065. doi:10.1200/JCO.2012.48.2752

    Article  PubMed  PubMed Central  Google Scholar 

  12. Chandwani KD, Thornton B, Perkins GH, Arun B, Raghuram NV, Nagendra HR, Wei Q, Cohen L (2010) Yoga improves quality of life and benefit finding in women undergoing radiotherapy for breast cancer. J Soc Integr Oncol 8(2):43–55

    PubMed  Google Scholar 

  13. Wengstrom Y, Haggmark C, Strander H, Forsberg C (2000) Perceived symptoms and quality of life in women with breast cancer receiving radiation therapy. Eur J Oncol Nurs 4(2):78–88. doi:10.1054/ejon.1999.0052 Discussion 89–90

    Article  CAS  PubMed  Google Scholar 

  14. Chen Z, Meng Z, Milbury K, Bei W, Zhang Y, Thornton B, Liao Z, Wei Q, Chen J, Guo X, Liu L, McQuade J, Kirschbaum C, Cohen L (2013) Qigong improves quality of life in women undergoing radiotherapy for breast cancer: results of a randomized controlled trial. Cancer 119(9):1690–1698. doi:10.1002/cncr.27904

    Article  PubMed  Google Scholar 

  15. Mock V, Dow KH, Meares CJ, Grimm PM, Dienemann JA, Haisfield-Wolfe ME, Quitasol W, Mitchell S, Chakravarthy A, Gage I (1997) Effects of exercise on fatigue, physical functioning, and emotional distress during radiation therapy for breast cancer. Oncol Nurs Forum 24(6):991–1000

    CAS  PubMed  Google Scholar 

  16. Palesh O, Peppone L, Innominato PF, Janelsins M, Jeong M, Sprod L, Savard J, Rotatori M, Kesler S, Telli M, Mustian K (2012) Prevalence, putative mechanisms, and current management of sleep problems during chemotherapy for cancer. Nature Sci sleep 4:151–162. doi:10.2147/NSS.S18895

    Article  Google Scholar 

  17. Otte JL, Carpenter JS, Russell KM, Bigatti S, Champion VL (2010) Prevalence, severity, and correlates of sleep-wake disturbances in long-term breast cancer survivors. J Pain Symptom Manag 39(3):535–547. doi:10.1016/j.jpainsymman.2009.07.004

    Article  Google Scholar 

  18. Davidson JR, MacLean AW, Brundage MD, Schulze K (2002) Sleep disturbance in cancer patients. Soc Sci Med 54(9):1309–1321

    Article  PubMed  Google Scholar 

  19. Phillips KM, Jim HS, Donovan KA, Pinder-Schenck MC, Jacobsen PB (2012) Characteristics and correlates of sleep disturbances in cancer patients. Supportive Care Cancer 20(2):357–365. doi:10.1007/s00520-011-1106-z

    Article  Google Scholar 

  20. Otte JL, Carpenter JS, Manchanda S, Rand KL, Skaar TC, Weaver M, Chernyak Y, Zhong X, Igega C, Landis C (2015) Systematic review of sleep disorders in cancer patients: can the prevalence of sleep disorders be ascertained? Cancer Med 4(2):183–200. doi:10.1002/cam4.356

    Article  PubMed  Google Scholar 

  21. Mishra SI, Scherer RW, Snyder C, Geigle PM, Berlanstein DR, Topaloglu O (2012) Exercise interventions on health-related quality of life for people with cancer during active treatment. Clin Otolaryngol 37(5):390–392

    Article  PubMed  Google Scholar 

  22. Jones LW, Alfano CM (2013) Exercise-oncology research: past, present, and future. Acta Oncol 52(2):195–215. doi:10.3109/0284186X.2012.742564

    Article  PubMed  Google Scholar 

  23. Schmitz KH, Courneya KS, Matthews C, Demark-Wahnefried W, Galvao DA, Pinto BM, Irwin ML, Wolin KY, Segal RJ, Lucia A, Schneider CM, von Gruenigen VE, Schwartz AL (2010) American college of sports medicine roundtable on exercise guidelines for cancer survivors. Med Sci Sports Exerc 42(7):1409–1426. doi:10.1249/MSS.0b013e3181e0c112

    Article  PubMed  Google Scholar 

  24. Sprod LK, Palesh OG, Janelsins MC, Peppone LJ, Heckler CE, Adams MJ, Morrow GR, Mustian KM (2010) Exercise, sleep quality, and mediators of sleep in breast and prostate cancer patients receiving radiation therapy. Commun Oncol 7(10):463–471

    Article  Google Scholar 

  25. Wenzel JA, Griffith KA, Shang J, Thompson CB, Hedlin H, Stewart KJ, DeWeese T, Mock V (2013) Impact of a home-based walking intervention on outcomes of sleep quality, emotional distress, and fatigue in patients undergoing treatment for solid tumors. Oncologist 18(4):476–484. doi:10.1634/theoncologist.2012-0278

    Article  PubMed  PubMed Central  Google Scholar 

  26. Potthoff K, Schmidt ME, Wiskemann J, Hof H, Klassen O, Habermann N, Beckhove P, Debus J, Ulrich CM, Steindorf K (2013) Randomized controlled trial to evaluate the effects of progressive resistance training compared to progressive muscle relaxation in breast cancer patients undergoing adjuvant radiotherapy: the BEST study. BMC Cancer 13:162. doi:10.1186/1471-2407-13-162

    Article  PubMed  PubMed Central  Google Scholar 

  27. Steindorf K, Schmidt ME, Klassen O, Ulrich CM, Oelmann J, Habermann N, Beckhove P, Owen R, Debus J, Wiskemann J, Potthoff K (2014) Randomized controlled trial of resistance training in breast cancer patients receiving adjuvant radiotherapy: results on cancer-related fatigue and quality of life. Ann Oncol. doi:10.1093/annonc/mdu374

    PubMed  Google Scholar 

  28. Schmidt ME, Meynkohn A, Habermann N, Wiskemann J, Oelmann J, Hof H, Wessels S, Klassen O, Debus J, Potthoff K, Steindorf K, Ulrich CM (2016) Resistance exercise and inflammation in breast cancer patients undergoing adjuvant radiation therapy: mediation analysis from a randomized, controlled intervention trial. Int J Radiat Oncol Biol Phys 94(2):329–337. doi:10.1016/j.ijrobp.2015.10.058

    Article  PubMed  Google Scholar 

  29. Klassen O, Schmidt ME, Scharhag-Rosenberger F, Sorkin M, Ulrich CM, Schneeweiss A, Potthoff K, Steindorf K, Wiskemann J (2014) Cardiorespiratory fitness in breast cancer patients undergoing adjuvant therapy. Acta Oncol 53(10):1356–1365. doi:10.3109/0284186X.2014.899435

    Article  CAS  PubMed  Google Scholar 

  30. Gollhofer S, Wiskemann J, Schmidt M, Klassen O, Ulrich C, Oelmann J, Hof H, Potthoff K, Steindorf K (2015) Factors influencing participation in a randomized controlled resistance exercise intervention study in breast cancer patients during radiotherapy. BMC Cancer 15(1):186

    Article  PubMed  PubMed Central  Google Scholar 

  31. Schmidt ME, Semik J, Habermann N, Wiskemann J, Ulrich CM, Steindorf K (2016) Cancer-related fatigue shows a stable association with diurnal cortisol dysregulation in breast cancer patients. Brain Behav Immun 52:98–105. doi:10.1016/j.bbi.2015.10.005

    Article  CAS  PubMed  Google Scholar 

  32. Ferguson JM, Marquis JN, Taylor CB (1977) A script for deep muscle relaxation. Dis Nerv Syst 38(9):703–708

    CAS  PubMed  Google Scholar 

  33. Beutel ME, Hinz A, Albani C, Brahler E (2006) Fatigue assessment questionnaire: standardization of a cancer-specific instrument based on the general population. Oncology 70(5):351–357

    Article  CAS  PubMed  Google Scholar 

  34. Aaronson NK, Ahmedzai S, Bergman B, Bullinger M, Cull A, Duez NJ, Filiberti A, Flechtner H, Fleishman SB, de Haes JC (1993) The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J Natl Cancer Inst 85(5):365–376

    Article  CAS  PubMed  Google Scholar 

  35. Weissman MM, Sholomskas D, Pottenger M, Prusoff BA, Locke BZ (1977) Assessing depressive symptoms in five psychiatric populations: a validation study. Am J Epidemiol 106(3):203–214

    Article  CAS  PubMed  Google Scholar 

  36. Dahlem NW, Zimet GD, Walker RR (1991) The multidimensional scale of perceived social support: a confirmation study. J Clin Psychol 47(6):756–761

    Article  CAS  PubMed  Google Scholar 

  37. Baron RM, Kenny DA (1986) The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol 51(6):1173–1182

    Article  CAS  PubMed  Google Scholar 

  38. MacKinnon DP, Luecken LJ (2011) Statistical analysis for identifying mediating variables in public health dentistry interventions. J Public Health Dent 71(Suppl 1):S37–S46

    Article  PubMed  PubMed Central  Google Scholar 

  39. Cerin E, Taylor LM, Leslie E, Owen N (2006) Small-scale randomized controlled trials need more powerful methods of mediational analysis than the Baron-Kenny method. J Clin Epidemiol 59(5):457–464. doi:10.1016/j.jclinepi.2005.11.008

    Article  PubMed  Google Scholar 

  40. MacKinnon DP, Lockwood CM, Hoffman JM, West SG, Sheets V (2002) A comparison of methods to test mediation and other intervening variable effects. Psychol Methods 7(1):83–104

    Article  PubMed  PubMed Central  Google Scholar 

  41. Freedman LS, Schatzkin A (1992) Sample size for studying intermediate endpoints within intervention trails or observational studies. Am J Epidemiol 136(9):1148–1159

    Article  CAS  PubMed  Google Scholar 

  42. Colagiuri B, Christensen S, Jensen AB, Price MA, Butow PN, Zachariae R (2011) Prevalence and predictors of sleep difficulty in a national cohort of women with primary breast cancer three to four months postsurgery. J Pain Symptom Manag 42(5):710–720. doi:10.1016/j.jpainsymman.2011.02.012

    Article  Google Scholar 

  43. Savard J, Liu L, Natarajan L, Rissling MB, Neikrug AB, He F, Dimsdale JE, Mills PJ, Parker BA, Sadler GR, Ancoli-Israel S (2009) Breast cancer patients have progressively impaired sleep-wake activity rhythms during chemotherapy. Sleep 32(9):1155–1160

    PubMed  PubMed Central  Google Scholar 

  44. Jim HS, Small B, Faul LA, Franzen J, Apte S, Jacobsen PB (2011) Fatigue, depression, sleep, and activity during chemotherapy: daily and intraday variation and relationships among symptom changes. Ann Behav Med 42(3):321–333

    Article  PubMed  PubMed Central  Google Scholar 

  45. Alfano CM, Lichstein KL, Vander Wal GS, Smith AW, Reeve BB, McTiernan A, Bernstein L, Baumgartner KB, Ballard-Barbash R (2011) Sleep duration change across breast cancer survivorship: associations with symptoms and health-related quality of life. Breast Cancer Res Treat 130(1):243–254

    Article  PubMed  PubMed Central  Google Scholar 

  46. Vadiraja SH, Rao MR, Nagendra RH, Nagarathna R, Rekha M, Vanitha N, Gopinath SK, Srinath B, Vishweshwara M, Madhavi Y, Basavalingaiah SA, Ramesh SB, Rao N (2009) Effects of yoga on symptom management in breast cancer patients: a randomized controlled trial. Int J Yoga 2(2):73–79. doi:10.4103/0973-6131.60048

    Article  PubMed  PubMed Central  Google Scholar 

  47. Cocks K, King MT, Velikova G, de Castro G Jr, Martyn St-James M, Fayers PM, Brown JM (2012) Evidence-based guidelines for interpreting change scores for the European Organisation for the Research and Treatment of Cancer Quality of Life Questionnaire Core 30. Eur J Cancer 48(11):1713–1721. doi:10.1016/j.ejca.2012.02.059

    Article  CAS  PubMed  Google Scholar 

  48. Courneya KS, Segal RJ, Mackey JR, Gelmon K, Friedenreich CM, Yasui Y, Reid RD, Jespersen D, Cook D, Proulx C, Trinh L, Dolan LB, Wooding E, Forbes CC, McKenzie DC (2014) Effects of exercise dose and type on sleep quality in breast cancer patients receiving chemotherapy: a multicenter randomized trial. Breast Cancer Res Treat 144(2):361–369. doi:10.1007/s10549-014-2883-0

    Article  CAS  PubMed  Google Scholar 

  49. Dodd MJ, Cho MH, Miaskowski C, Painter PL, Paul SM, Cooper BA, Duda J, Krasnoff J, Bank KA (2010) A randomized controlled trial of home-based exercise for cancer-related fatigue in women during and after chemotherapy with or without radiation therapy. Cancer Nurs 33(4):245–257. doi:10.1097/NCC.0b013e3181ddc58c

    Article  PubMed  PubMed Central  Google Scholar 

  50. Wang YJ, Boehmke M, Wu YW, Dickerson SS, Fisher N (2011) Effects of a 6-week walking program on Taiwanese women newly diagnosed with early-stage breast cancer. Cancer Nurs 34(2):E1–E13. doi:10.1097/NCC.0b013e3181e4588d

    Article  PubMed  Google Scholar 

  51. Yang CY, Tsai JC, Huang YC, Lin CC (2011) Effects of a home-based walking program on perceived symptom and mood status in postoperative breast cancer women receiving adjuvant chemotherapy. J Adv Nurs 67(1):158–168. doi:10.1111/j.1365-2648.2010.05492.x

    Article  PubMed  Google Scholar 

  52. Minton O, Stone PC (2012) A comparison of cognitive function, sleep and activity levels in disease-free breast cancer patients with or without cancer-related fatigue syndrome. BMJ Support Palliat Care 2(3):231–238. doi:10.1136/bmjspcare-2011-000172

    Article  PubMed  PubMed Central  Google Scholar 

  53. Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res 28(2):193–213

    Article  CAS  PubMed  Google Scholar 

  54. Kline CE (2014) The bidirectional relationship between exercise and sleep: implications for exercise adherence and sleep improvement. Am J Lifestyle Med 8(6):375–379. doi:10.1177/1559827614544437

    Article  PubMed  PubMed Central  Google Scholar 

  55. Driver HS, Taylor SR (2000) Exercise and sleep. Sleep Med Rev 4(4):387–402. doi:10.1053/smrv.2000.0110

    Article  PubMed  Google Scholar 

  56. Kline CE, Irish LA, Krafty RT, Sternfeld B, Kravitz HM, Buysse DJ, Bromberger JT, Dugan SA, Hall MH (2013) Consistently high sports/exercise activity is associated with better sleep quality, continuity and depth in midlife women: the SWAN sleep study. Sleep 36(9):1279–1288. doi:10.5665/sleep.2946

    PubMed  PubMed Central  Google Scholar 

  57. Jain S, Boyd C, Fiorentino L, Khorsan R, Crawford C (2015) Are there efficacious treatments for treating the fatigue-sleep disturbance-depression symptom cluster in breast cancer patients? A Rapid Evidence Assessment of the Literature (REAL©). Breast Cancer (Dove Med Press) 7:267–291. doi:10.2147/BCTT.S25014

    Google Scholar 

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Acknowledgements

We would like to thank the patients who participated in this clinical trial. We also thank the Institute of Sports and Sports Science of the University of Heidelberg for providing the training facilities; Lena Kempf, Marcel Bannasch, Nadine Ungar, and Beate Biazeck for performing the interventions; Karin Potthoff, MD, Jan Oelmann, MD, Ulrike Bussas, MD, Simone Hummler, MD, Holger Hof, MD, and Andrea Koffka, MD, for medical support and/or help with recruitment; Oliver Klassen, PhD, Sabine Wessels, PhD, and Sandra Gollhofer, MD, for study assistance; Werner Diehl, PhD, for data management, and Christina Bock, PhD, for helping with searching literature.

Funding

This work was supported by the Interdisciplinary Research Funding Program (intramural) of the National Center for Tumor Diseases (NCT), Heidelberg, Germany. The foundation “Stiftung Leben mit Krebs” partially supported the intervention programs and the foundation “Manfred-Lautenschlaeger-Stiftung” supported JW.

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Correspondence to Karen Steindorf.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Informed consent was obtained from all individual participants included in the study.

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Steindorf, K., Wiskemann, J., Ulrich, C.M. et al. Effects of exercise on sleep problems in breast cancer patients receiving radiotherapy: a randomized clinical trial. Breast Cancer Res Treat 162, 489–499 (2017). https://doi.org/10.1007/s10549-017-4141-8

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