Support Care Cancer (2014) 22:2535–2545 DOI 10.1007/s00520-014-2204-5
ORIGINAL ARTICLE
Sleep, fatigue, depression, and circadian activity rhythms in women with breast cancer before and after treatment: a 1-year longitudinal study Sonia Ancoli-Israel & Lianqi Liu & Michelle Rissling & Loki Natarajan & Ariel B. Neikrug & Barton W. Palmer & Paul J. Mills & Barbara A. Parker & Georgia Robins Sadler & Jeanne Maglione
Received: 16 September 2013 / Accepted: 9 March 2014 / Published online: 15 April 2014 # Springer-Verlag Berlin Heidelberg 2014
Abstract Purpose Sleep disturbance, fatigue and depression are common complaints in patients with cancer, and often contribute to worse quality of life (QoL). Circadian activity rhythms (CARs) are often disrupted in cancer patients. These symptoms worsen during treatment, but less is known about their long-term trajectory. S. Ancoli-Israel (*) : L. Liu : M. Rissling : A. B. Neikrug : B. W. Palmer : P. J. Mills : J. Maglione Department of Psychiatry, University of California, San Diego, 9500 Gilman Drive, La Jolla, CA, USA e-mail:
[email protected] S. Ancoli-Israel : B. A. Parker Department of Medicine, University of California, San Diego, La Jolla, CA, USA L. Natarajan Department of Family and Preventive Medicine, University of California, San Diego, La Jolla, CA, USA G. R. Sadler Department of Surgery, University of California, San Diego, La Jolla, CA, USA S. Ancoli-Israel : M. Rissling : L. Natarajan : A. B. Neikrug : B. W. Palmer : P. J. Mills SDSU/UCSD Joint Doctoral Program in Clinical Psychology, San Diego, CA, USA S. Ancoli-Israel : L. Natarajan : B. A. Parker : G. R. Sadler UCSD Moores Cancer Center, La Jolla, CA, USA L. Liu Veterans Affairs San Diego Healthcare System, San Diego, CA, USA S. Ancoli-Israel : L. Liu VA Center of Excellence for Stress and Mental Health, San Diego, CA, USA
Methods Sixty-eight women with stage I-III breast cancer (BC) scheduled to receive ≥4 cycles of chemotherapy, and age-, ethnicity-, and education-matched normal, cancer-free controls (NC) participated. Sleep was measured with actigraphy (nocturnal total sleep time [nocturnal TST] and daytime total nap time [NAPTIME]) and with the Pittsburgh Sleep Quality Index (PSQI); fatigue with the Multidimensional Fatigue Symptom Inventory-Short Form (MFSI-SF); depression with the Center of Epidemiological Studies-Depression (CES-D). CARs were derived from actigraphy. Several measures of QoL were administered. Data were collected at three time points: before (baseline), end of cycle 4 (cycle 4), and 1 year post-chemotherapy (1 year). Results Compared to NC, BC had longer NAPTIME, worse sleep quality, more fatigue, more depressive symptoms, more disrupted CARs, and worse QoL at baseline (all p values 0.06). Reported medical comorbidities over time are listed in Table 2. At baseline, there were no significant group differences for any of the reported diseases (all p values >0.06). There were also no significant changes across the three time points in each group for any of the diseases (all p values >0.06).
2539 Table 1 Demographic and disease characteristics Characteristics Age (years) Mean (SD) Range Body mass index (BMI, kg/m2) Mean (SD) Range Race [n (%)] Caucasian Non-Caucasian Education [n (%)] Below completed college Completed college and above Marital status [n (%)] Never married Divorced/separated/widowed Married Household annual income [n (%)] ≤ $100,000 > $100,000 Baseline menopausal status [n (%)] Premenopause Perimenopause Postmenopause Hysterectomy Not available Cancer stage [n (%)] Stage I Stage II Stage III Not available Surgery type Lumpectomy Mastectomy Double mastectomy No surgery before Chemotherapy Not available Days between surgery and start of chemotherapy Available (n=47) Mean (SD) Range Not available (n=21) Chemotherapy regimen [n (%)] AC AC followed by docetaxel AC followed by paclitaxel Other Not available
BC (n=68)
NC (n=60)
51.3 (9.1) 31–76
52.4 (9.4) 29–81
27.6 (7.4) 19.3–61.9
25.9 (7.0) 19.1–56.7
60 (88.2) 8 (11.8)
51 (85.0) 9 (15.0)
32 (47.1) 36 (52.9)
21 (35.0) 39 (65.0)
3 (4.4) 19 (27.9) 46 (67.7)
7 (11.7) 12 (20.0) 41 (68.3)
25 (36.8) 43 (63.2)
21 (35.0) 39 (65.0)
28 (41.2) 8 (11.8) 27 (39.7) 5 (7.3) 0
20 (33.9) 8 (13.6) 22 (37.3) 9 (15.3) 1 –
19 (28.4) 27 (40.3) 21 (31.3) 1 – 31 (45.6) 31 (45.3) 3 (4.4) 3 (4.4) 0 – 42.0 (16.7) 14–106 – – 13 (19.7) 6 (9.1) 34 (51.5) 13 (19.7) 2
No significant differences between the two groups in age, BMI, race, education, marital status, household annual income, and baseline menopause status (all p values >0.2) AC Doxorubicin+Cyclophosphamide, BC women with breast cancer, NC cancer-free controls
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Support Care Cancer (2014) 22:2535–2545
Table 2 Medical comorbidities over time [n (%)] Diseases
Baseline
Cycle 4
1 Year
BC (n=66)
NC (n=55)
BC (n=58)
NC (n=49)
BC (n=41)
NC (n=28)
Cardiovascular diseases Pulmonary diseases Central nervous diseases Gastrointestinal diseases Renal disease Endocrine disease Connective tissue diseases Infections Dementia Arthritis Diabetes Ulcer Hiatal hernia Esophageal diseases
2 (3.0) 0 (0.0) 0 (0.0) 4 (6.1) 0 (0.0) 5 (7.6) 1 (1.5) 3 (4.6) 0 (0.0) 8 (12.2) 4 (6.1) 2 (3.0) 0 (0.0) 1 (1.5)
0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 4 (7.3) 0 (0.0) 0 (0.0) 1 (1.8) 0 (0.0)
2 (3.5) 1 (1.7) 0 (0.0) 2 (3.5) 0 (0.0) 1 (1.7) 2 (3.5) 2 (3.5) 0 (0.0) 6 (10.3) 3 (5.2) 1 (1.7) 0 (0.0) 1 (1.7)
0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2 (4.1) 0 (0.0) 2 (4.1) 0 (0.0) 5 (10.2) 0 (0.0) 0 (0.0) 1 (2.4) 0 (0.0)
1 (2.4) 1 (2.4) 1 (2.4) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 2 (4.9) 0 (0.0) 11 (26.8) 2 (4.9) 1 (2.4) 2 (4.9) 0 (0.0)
0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 1 (3.6) 0 (0.0) 1 (3.6) 0 (0.0) 7 (25.0) 1 (3.6) 0 (0.0) 0 (0.0) 0 (0.0)
Neck/back/spine problems Epilepsy Headaches High blood pressure Kidney problems Stroke Asthma Emphysema Edema Thyroid disease Other diseases
10 (15.2) 0 (0.0) 12 (18.2) 10 (15.2) 0 (0.0) 0 (0.0) 6 (9.1) 0 (0.0) 2 (3.0) 12 (18.2) 8 (12.2)
9 (16.4) 0 (0.0) 6 (10.9) 11 (20.0) 0 (0.0) 1 (1.8) 3 (5.5) 0 (0.0) 0 (0.0) 3 (5.5) 4 (7.3)
10 (17.2) 1 (1.7) 15 (25.9) 8 (13.8) 0 (0.0) 1 (1.7) 6 (10.3) 0 (0.0) 3 (5.2) 10 (17.2) 13 (22.4)
11 (22.5) 0 (0.0) 5 (10.2) 11 (22.5) 0 (0.0) 0 (0.0) 4 (8.2) 0 (0.0) 1 (2.4) 4 (8.2) 1 (2.4)
9 (21.9) 1 (2.4) 12 (29.3) 8 (19.5) 0 (0.0) 0 (0.0) 3 (7.3) 1 (2.4) 2 (4.9) 8 (19.5) 6 (14.6)
6 (21.4) 0 (0.0) 6 (21.4) 7 (25.0) 0 (0.0) 0 (0.0) 1 (3.6) 0 (0.0) 1 (3.6) 3 (10.7) 2 (7.1)
Data for 2 BC and 5 NC were not available at baseline; 8 more BC and 6 more NC at cycle 4, and 25 more BC and 27 more NC at 1 year were either dropped or stopped due to the end of study. There were no significant group differences at baseline (all p values >0.5); and no changes over time in both groups for all disease (all p values >0.06) BC breast cancer patients, NC cancer-free controls
Sleep Objective measures Nocturnal TST There were no significant differences in nocturnal TST between BC and NC at any time points; nor were there any significant changes over time in either group (see Table 3). NAPTIME Mixed model analysis showed that there was a significant group effect (p=0.0008); further post hoc testing of between group differences at each time point indicated that compared to NC, BC spent more time napping at baseline (p= 0.0095) and cycle 4 (p0.1) (see Table 3). Subjective measures Total PSQI scores are shown in Fig. 2a. Mixed model analysis showed that there was a significant group effect (p
