Abstract
Purpose
The purpose of this study was to examine patterns of circadian activity rhythms and their relationship with fatigue, anxiety/depression, and demographic/medical variables in women receiving breast cancer adjuvant therapy treatments (Tx) at three times within a randomized clinical trial (RCT) designed to improve sleep and modify fatigue.
Methods
A RCT enrolled 219 women with stage I–IIIA breast cancer who were randomized 2 days prior to starting chemotherapy to a behavioral therapy sleep intervention or healthy eating control group. All cases with available data (n = 190) were included in a descriptive, correlational, repeated measures analysis. Activity data were collected continuously by wrist actigraphy for 7 days at three times: the start (Tx 1), continuation (Tx 3), and recovery (30 days after last Tx) of chemotherapy. Circadian activity rhythm parameters were generated using Action4 software (Ambulatory Monitoring, Inc.). Measures collected simultaneously included Piper Fatigue Scale, Hospital Anxiety and Depression Scale, and demographic/medical variables.
Results
Circadian activity rhythm parameters at three times in both groups were disrupted compared to healthy adults, but similar to values of cancer patients. Significant changes in mesor, amplitude, peak activity, and 24 h autocorrelation values were found over time in both groups. The intervention group’s amplitude and circadian quotient values were significantly more robust. More robust activity rhythms were associated with lower fatigue, depressive symptoms, body mass index, and higher performance status in both groups.
Conclusions
Disrupted patterns of circadian activity rhythms were prevalent and associated with distressing fatigue and depressive symptoms during chemotherapy and at recovery. The intervention resulted in more robust rhythms.
Similar content being viewed by others
References
Acebo C, LeBourgeois MK (2006) Actigraphy. Respir Care Clin N Am 12(1):23
Ancoli-Israel S, Cole R, Alessi C, Chambers M, Moorcroft W, Pollak CP (2003) The role of actigraphy in the study of sleep and circadian rhythms. Sleep 26(3):342–392
Ancoli-Israel S, Klauber MR, Jones DW, Kripke DF, Martin J, Mason W et al (1997) Variations in circadian rhythms of activity, sleep, and light exposure related to dementia in nursing-home patients. Sleep 20(1):18–23
Ancoli-Israel S, Liu L, Marler MR, Parker BA, Jones V, Sadler GR et al (2006) Fatigue, sleep, and circadian rhythms prior to chemotherapy for breast cancer. Support Care Cancer 14(3):201–209. doi:10.1007/s00520-005-0861-0
Berger AM (1998) Patterns of fatigue and activity and rest during adjuvant breast cancer chemotherapy. Oncol Nurs Forum 25(1):51–62
Berger AM, Farr L (1999) The influence of daytime inactivity and nighttime restlessness on cancer-related fatigue. Oncol Nurs Forum 26(10):1663–1671
Berger AM, Farr LA, Kuhn BR, Fischer P, Agrawal S (2007) Values of sleep/wake, activity/rest, circadian rhythms, and fatigue prior to adjuvant breast cancer chemotherapy. J Pain Symptom Manage 33(4):398–409. doi:10.1016/j.jpainsymman.2006.09.022
Berger AM, Higginbotham P (2000) Correlates of fatigue during and following adjuvant breast cancer chemotherapy: a pilot study. Oncol Nurs Forum 27(9):1443–1448
Berger AM, Kuhn BR, Farr LA, Lynch JC, Agrawal S, Chamberlain JA et al (2008) Behavioral therapy intervention trial to improve sleep quality and cancer-related fatigue. Psycho-oncology. doi:10.1002/pon.1438 online 12/17/08 PMID 19090531
Berger AM, VonEssen S, Kuhn BR, Piper BF, Agrawal S, Lynch JC et al (2003) Adherence, sleep, and fatigue outcomes after adjuvant breast cancer chemotherapy: results of a feasibility intervention study. Oncol Nurs Forum 30(3):513–522. doi:10.1188/03.ONF.513-522
Berger AM, Wielgus K, Young-McCaughan S, Fischer P, Farr L, Lee KA (2008) Methodological challenges when using actigraphy in research. J Pain Symptom Manage 36(2):191–199. doi:10.1016/j.jpainsymman.2007.10.008
Brown AC, Smolensky MH, D'Alonzo GE, Redman DP (1990) Actigraphy: a means of assessing circadian patterns in human activity. Chronobiol Int 7(2):125–133. doi:10.3109/07420529009056964
Buysse DJ, Reynolds CF, 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. doi:10.1016/0165-1781(89) 90047-4
Chevalier V, Mormont MC, Cure H, Chollet P (2003) Assessment of circadian rhythms by actimetry in healthy subjects and patients with advanced colorectal cancer. Oncol Rep 10(3):733–737
Cole RJ, Kripke DF, Gruen W, Mullaney DJ, Gillin JC (1992) Automatic sleep/wake identification from wrist activity. Sleep 15(5):461–469
de Souza L, Benedito-Silva AA, Pires ML, Poyares D, Tufik S, Calil HM (2003) Further validation of actigraphy for sleep studies. Sleep 26(1):81–85
Dijk DJ, von Schantz M (2005) Timing and consolidation of human sleep, wakefulness, and performance by a symphony of oscillators. J Biol Rhythms 20(4):279–290. doi:10.1177/0748730405278292
Donovan KA, Small BJ, Andrykowski MA, Munster P, Jacobsen PB (2007) Utility of a cognitive–behavioral model to predict fatigue following breast cancer treatment. Health Psychol Off J Of The Div Of Health Psychol Am Psychol Assoc 26(4):464–472
Dzaja A, Arber S, Hislop J, Kerkhofs M, Kopp C, Pollmacher T et al (2005) Women's sleep in health and disease. J Psychiatr Res 39(1):55–76. doi:10.1016/j.jpsychires.2004.05.008
Farr L, Boen L (1996) Comparison of rectal and axillary temperature rhythms with activity. Paper presented at the NASA Space Grant Consortium Symposium, Lincoln, NE
Fernandes R, Stone P, Andrews P, Morgan R, Sharma S (2006) Comparison between fatigue, sleep disturbance, and circadian rhythm in cancer inpatients and healthy volunteers: evaluation of diagnostic criteria for cancer-related fatigue. J Pain Symptom Manage 32(3):245–254. doi:10.1016/j.jpainsymman.2006.03.014
Lanuza D, Farr L (2003) Circadian rhythm disorders. In: Carrieri-Kohlman VA, Lindsey A, West C (eds) Pathophysiological phenomena in nursing, 3rd edn. Saunders, St Louis, MO, pp 65–90
Lentz MJ (1990) Time-series analysis–cosinor analysis: a special case. West J Nurs Res 12(3):408–412. doi:10.1177/019394599001200313
Levin RD, Daehler MA, Grutsch JF, Quiton J, Lis CG, Peterson C et al (2005) Circadian function in patients with advanced non-small-cell lung cancer. Br J Cancer 93(11):1202–1208. doi:10.1038/sj.bjc.6602859
Lichstein KL, Stone KC, Donaldson J, Nau SD, Soeffing JP, Murray D et al (2006) Actigraphy validation with insomnia. Sleep 29(2):232–239
Littner M, Kushida CA, Anderson WM, Bailey D, Berry RB, Davila DG et al (2003) Practice parameters for the role of actigraphy in the study of sleep and circadian rhythms: an update for 2002. Sleep 26(3):337–341
Mitchell SA, Beck SL, Hood LE, Moore K, Tanner ER (2007) Putting evidence into practice: evidence-based interventions for fatigue during and following cancer and its treatment. Clin J Oncol Nurs 11(1):99–113. doi:10.1188/07.CJON.99-113
Mock V, Atkinson A, Barsevick AM, Berger AM, Cimprich B, Eisenberger MA et al (2007) Cancer-related fatigue. Clinical practice guidelines in oncology. J Natl Compr Cancer Netw 5(10):1054–1078
Monk TH (2005) Aging human circadian rhythms: conventional wisdom may not always be right. J Biol Rhythms 20(4):366–374. doi:10.1177/0748730405277378
Mor V, Laliberte L, Morris JN, Wiemann M (1984) The Karnofsky Performance Status Scale. An examination of its reliability and validity in a research setting. Cancer 53(9):2002–2007. doi:10.1002/1097-0142(19840501)53:9<2002::AID-CNCR2820530933>3.0.CO;2-W
Morgenthaler T, Alessi C, Friedman L, Owens J, Kapur V, Boehlecke B et al (2007) Practice parameters for the use of actigraphy in the assessment of sleep and sleep disorders: an update for 2007. Sleep 30(4):519–529
Mormont MC, Langouet AM, Claustrat B, Bogdan A, Marion S, Waterhouse J et al (2002) Marker rhythms of circadian system function: a study of patients with metastatic colorectal cancer and good performance status. Chronobiol Int 19(1):141–155. doi:10.1081/CBI-120002593
Mormont MC, Waterhouse J (2002) Contribution of the rest-activity circadian rhythm to quality of life in cancer patients. Chronobiol Int 19(1):313–323. doi:10.1081/CBI-120002606
Mormont MC, Waterhouse J, Bleuzen P, Giacchetti S, Jami A, Bogdan A et al (2000) Marked 24 h rest/activity rhythms are associated with better quality of life, better response, and longer survival in patients with metastatic colorectal cancer and good performance status. Clin Cancer Res 6(8):3038–3045
Mullaney DJ, Kripke DF, Messin S (1980) Wrist-actigraphic estimation of sleep time. Sleep 3(1):83–92
Mustian KM, Morrow GR, Carroll JK, Figueroa-Moseley CD, Jean-Pierre P, Williams GC (2007) Integrative nonpharmacologic behavioral interventions for the management of cancer-related fatigue. Oncologist 12(Suppl 1):52–67. doi:10.1634/theoncologist.12-S1-52
Piper BF, Dibble SL, Dodd MJ, Weiss MC, Slaughter RE, Paul SM (1998) The revised Piper Fatigue Scale: psychometric evaluation in women with breast cancer. Oncol Nurs Forum 25(4):677–684
Rich T, Innominato PF, Boerner J, Mormont MC, Iacobelli S, Baron B et al (2005) Elevated serum cytokines correlated with altered behavior, serum cortisol rhythm, and dampened 24 hour rest-activity patterns in patients with metastatic colorectal cancer. Clin Cancer Res 11(5):1757–1764. doi:10.1158/1078-0432.CCR-04-2000
Roscoe JA, Morrow GR, Hickok JT, Bushunow P, Matteson S, Rakita D et al (2002) Temporal interrelationships among fatigue, circadian rhythm and depression in breast cancer patients undergoing chemotherapy treatment. Support Care Cancer 10(4):329–336. doi:10.1007/s00520-001-0317-0
Sephton S, Spiegel D (2003) Circadian disruption in cancer: a neuroendocrine-immune pathway from stress to disease? Brain Behav Immun 17(5):321–328. doi:10.1016/S0889-1591(03) 00078-3
Snaith RP (2003) The hospital anxiety and depression scale. Health Qual Life Outcomes 1:29. doi:10.1186/1477-7525-1-29
Teychenne M, Ball K, Salmon J (2008) Physical activity and likelihood of depression in adults: a review. Prev Med 46(5):397–411. doi:10.1016/j.ypmed.2008.01.009
Van Gelder RN (2004) Recent insights into mammalian circadian rhythms. Sleep 27(1):166–171
Zigmond AS, Snaith RP (1983) The hospital anxiety and depression scale. Acta Psychiatr Scand 67(6):361–370. doi:10.1111/j.1600-0447.1983.tb09716.x
Acknowledgments
The authors thank the National Institute of Health/National Institute of Nursing Research for support for this study (5R01NR007762-05). We also thank the physicians, nurses, and staff at all participating sites, especially the University of Nebraska Medical Center/Eppley Cancer Center, Nebraska Cancer Specialists/ Methodist Estabrook Cancer Center, and Southeast Nebraska Hematology/Oncology Consultants
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Berger, A.M., Wielgus, K., Hertzog, M. et al. Patterns of circadian activity rhythms and their relationships with fatigue and anxiety/depression in women treated with breast cancer adjuvant chemotherapy. Support Care Cancer 18, 105–114 (2010). https://doi.org/10.1007/s00520-009-0636-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00520-009-0636-0