Abstract
Purpose
Sleep disturbance and cancer-related fatigue (CRF) are among the most commonly reported symptoms associated with breast cancer and its treatment. This study identified symptom cluster groups of breast cancer patients based on multidimensional assessment of sleep disturbance and CRF prior to and during chemotherapy.
Methods
Participants were 152 women with stage I–IIIA breast cancer. Data were collected before chemotherapy (T1) and during the final week of the fourth chemotherapy cycle (T2). Latent profile analysis was used to derive groups of patients at each timepoint who scored similarly on percent of the day/night asleep per actigraphy, the Pittsburgh Sleep Quality Index global score, and the five subscales of the Multidimensional Fatigue Symptom Inventory-Short Form. Bivariate logistic regression evaluated if sociodemographic/medical characteristics at T1 were associated with group membership at each timepoint.
Results
Three groups (Fatigued with sleep complaints, Average, Minimal symptoms) were identified at T1, and five groups (Severely fatigued with poor sleep, Emotionally fatigued with average sleep, Physically fatigued with average sleep, Average, Minimal symptoms) at T2. The majority of individuals in a group characterized by more severe symptoms at T1 were also in a more severe symptom group at T2. Sociodemographic/medical variables at T1 were significantly associated with group membership at T1 and T2.
Conclusions
This study identified groups of breast cancer patients with differentially severe sleep disturbance and CRF symptom profiles prior to and during chemotherapy. Identifying groups with different symptom management needs and distinguishing groups by baseline sociodemographic/medical variables can identify patients at risk for greater symptom burden.
Similar content being viewed by others
References
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. https://doi.org/10.1200/JCO.2009.22.5011
Bower JE (2014) Cancer-related fatigue—mechanisms, risk factors, and treatments. Nat Rev Clin Oncol 11:597–609. https://doi.org/10.1038/nrclinonc.2014.127
Berger AM, Mooney K, Alvarez-Perez A, Breitbart WS, Carpenter KM, Cella D, Cleeland C, Dotan E, Eisenberger MA, Escalante CP, Jacobsen PB, Jankowski C, LeBlanc T, Ligibel JA, Loggers ET, Mandrell B, Murphy BA, Palesh O, Pirl WF, Plaxe SC, Riba MB, Rugo HS, Salvador C, Wagner LI, Wagner-Johnston ND, Zachariah FJ, Bergman MA, Smith C, National comprehensive cancer network (2015) Cancer-related fatigue, version 2.2015. J Natl Compr Cancer Netw 13(8):1012–1039
de Jong N, Courtens AM, Abu-Saad HH, Schouten HC (2002) Fatigue in patients with breast cancer receiving adjuvant chemotherapy: a review of the literature. Cancer Nurs 25(4):283–297
Bennett B, Goldstein D, Friedlander M, Hickie I, Lloyd A (2007) The experience of cancer-related fatigue and chronic fatigue syndrome: a qualitative and comparative study. J Pain Symptom Manag 34(2):126–135. https://doi.org/10.1016/j.jpainsymman.2006.10.014
Roscoe JA, Kaufman ME, Matteson-Rusby SE, Palesh OG, Ryan JL, Kohli S, Perlis ML, Morrow GR (2007) Cancer-related fatigue and sleep disorders. Oncologist 12(Suppl 1):35–42. https://doi.org/10.1634/theoncologist.12-S1-35
Abrahams HJG, Gielissen MFM, Verhagen CAHHVM, Knoop H (2018) The relationship of fatigue in breast cancer survivors with quality of life and factors to address in psychological interventions: a systematic review. Clin Psychol Rev 63:1–11. https://doi.org/10.1016/j.cpr.2018.05.004
Dickerson SS, Connors LM, Fayad A, Dean GE (2014) Sleep–wake disturbances in cancer patients: narrative review of literature focusing on improving quality of life outcomes. Nat Sci Sleep 6:85–100. https://doi.org/10.2147/NSS.S34846
Gallicchio L, Kalesan B (2009) Sleep duration and mortality: a systematic review and meta-analysis. J Sleep Res 18(2):148–158. https://doi.org/10.1111/j.13652869.2008.00732.x
Miaskowski C, Barsevick A, Berger A, Casagrande R, Grady PA, Jacobsen P, Kutner J, Patrick D, Zimmerman L, Xiao C, Matocha M, Marden S (2017) Advancing symptom science through symptom cluster research: expert panel proceedings and recommendations. J Natl Cancer Inst 109(4):djw253. https://doi.org/10.1093/jnci/djw253
Dodd MJ, Cho MH, Cooper BA, Petersen J, Bank KA, Lee KA, Miaskowski C (2011) Identification of latent classes in patients who are receiving biotherapy based on symptom experience and its effect on functional status and quality of life. Oncol Nurs Forum 38(1):33–42. https://doi.org/10.1188/11.ONF.33-42
Doong SH, Dhruva A, Dunn LB, West C, Paul SM, Cooper BA, Elboim C, Abrams G, Merriman JD, Langford DJ, Leutwyler H, Baggott C, Kober K, Aouizerat BE, Miaskowski C (2015) Associations between cytokine genes and a symptom cluster of pain, fatigue, sleep disturbance, and depression in patients prior to breast cancer surgery. Biol Res Nurs 17(3):237–247. https://doi.org/10.1177/1099800414550394
Illi J, Miaskowski C, Cooper B, Levine JD, Dunn L, West C, Dodd M, Dhruva A, Paul SM, Baggott C, Cataldo J, Langford D, Schmidt B, Aouizerat BE (2012) Association between pro- and anti-inflammatory cytokine genes and a symptom cluster of pain, fatigue, sleep disturbance, and depression. Cytokine 58(3):437–447. https://doi.org/10.1016/j.cyto.2012.02.015
Miaskowski C, Cooper BA, Melisko M, Chen LM, Mastick J, West C, Paul SM, Dunn LB, Schmidt BL, Hammer M, Cartwright F, Wright F, Langford DJ, Lee K, Aouizerat BE (2014) Disease and treatment characteristics do not predict symptom occurrence profiles in oncology outpatients receiving chemotherapy. Cancer 120(15):2371–2378. https://doi.org/10.1002/cncr.28699
Miaskowski C, Dunn L, Ritchie C, Paul SM, Cooper B, Aouizerat BE, Alexander K, Skerman H, Yates P (2015) Latent class analysis reveals distinct subgroups of patients based on symptom occurrence and demographic and clinical characteristics. J Pain Symptom Manag 50(1):28–37. https://doi.org/10.1016/j.jpainsymman.2014.12.011
Trudel-Fitzgerald C, Savard J, Ivers H (2014) Longitudinal changes in clusters of cancer patients over an 18-month period. Health Psychol 33(9):1012–1022. https://doi.org/10.1037/a0033497
O’Donnell D, Silva EJ, Munch M et al (2009) Comparison of subjective and objective assessments of sleep in healthy older subjects without sleep complaints. J Sleep Res 18(2):254–263. https://doi.org/10.1111/j.1365-2869.2008.00719.x
Thong MSY, Mols F, van de Poll-Franse LV et al (2018) Identifying the subtypes of cancer-related fatigue: results from the population-based PROFILES registry. J Cancer Surviv 12(1):38–46. https://doi.org/10.1007/s11764-017-0641-0
Dirksen SR, Belyea MJ, Epstein DR (2009) Fatigue-based subgroups of breast cancer survivors with insomnia. Cancer Nurs 32(5):404–411. https://doi.org/10.1097/NCC.0b013e3181a5d05e
Bower JE, Wiley J, Petersen L, Irwin MR, Cole SW, Ganz PA (2018) Fatigue after breast cancer treatment: biobehavioral predictors of fatigue trajectories. Health Psychol 37(11):1025–1034. https://doi.org/10.1037/hea0000652
Van Onselen C, Cooper BA, Lee K et al (2012) Identification of distinct subgroups of breast cancer patients based on self-reported changes in sleep disturbance. Support Care Cancer 20(10):2611–2619. https://doi.org/10.1007/s00520-012-1381-3
Ancoli-Israel S, Liu L, Marler MR, Parker BA, Jones V, Sadler GR, Dimsdale J, Cohen-Zion M, Fiorentino L (2006) Fatigue, sleep, and circadian rhythms prior to chemotherapy for breast cancer. Support Care Cancer 14(3):201–209. https://doi.org/10.1007/s00520-005-0861-0
Ancoli-Israel S, Liu L, Rissling M, Natarajan L, Neikrug AB, Palmer BW, Mills PJ, Parker BA, Sadler GR, Maglione J (2014) Sleep, fatigue, depression, and circadian activity rhythms in women with breast cancer before and after treatment: a 1-year longitudinal study. Support Care Cancer 22(9):2535–2545. https://doi.org/10.1007/s00520-014-2204-5
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, Martin JL, Blackwell T, Buenaver L, Liu L, Meltzer LJ, Sadeh A, Spira AP, Taylor DJ (2015) The SBSM guide to actigraphy monitoring: clinical and research applications. Behav Sleep Med 13(sup1):S4–S38. https://doi.org/10.1080/15402002.2015.1046356
Lichstein KL, Stone KC, Donaldson J, Nau SD, Soeffing JP, Murray D, Lester KW, Aguillard RN (2006) Actigraphy validation with insomnia. Sleep 29(2):232–239
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
Stein KD, Martin SC, Hann DM, Jacobsen PB (1998) A multidimensional measure of fatigue for use with cancer patients. Cancer Pract 6(3):143–152
Stein KD, Jacobsen PB, Blanchard CM, Thors C (2004) Further validation of the Multidimensional Fatigue Symptom Inventory-Short Form. J Pain Symptom Manag 27(1):14–23
Hill AL, Degnan KA, Calkins SD, Keane SP (2006) Profiles of externalizing behavior problems for boys and girls across preschool: the roles of emotion regulation and inattention. Dev Psychol 42(5):913–928. https://doi.org/10.1037/0012-1649.42.5.913
Muthén LK, Muthén BO (1998-2011) Mplus User’s guide. Sixth edition. Muthén & Muthén, Los Angeles
Enders CK (2010) Applied missing data analysis. Guilford Press, New York
Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19(6):716–723. https://doi.org/10.1109/TAC.1974.1100705
Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6(2):461–464
Arminger G, Stein P, Wittenberg J (1999) Mixtures of conditional mean-and covariance-structure models. Psychometrika 64(4):475–494. https://doi.org/10.1007/BF02294568
McLachlan G, Peel D (2004) Finite mixture models. John Wiley & Sons
Ramaswamy V, DeSarbo WS, Reibstein DJ, Robinson WT (1993) An empirical pooling approach for estimating marketing mix elasticities with PIMS data. Mark Sci 12(1):103–124
Roesch SC, Villodas M, Villodas F (2010) Latent class/profile analysis in maltreatment research: a commentary on Nooner et al., Pears et al., and looking beyond. Child Abuse Negl 34(3):155–160. https://doi.org/10.1016/j.chiabu.2010.01.003
Edinger JD, Bonnet MH, Bootzin RR, Doghramji K, Dorsey CM, Espie CA, Jamieson AO, McCall W, Morin CM, Stepanski EJ, American Academy of Sleep Medicine Work Group (2004) Derivation of research diagnostic criteria for insomnia: report of an American Academy of Sleep Medicine Work Group. Sleep 27(8):1567–1596
Beck SL, Schwartz AL, Towsley G, Dudley W, Barsevick A (2004) Psychometric evaluation of the Pittsburgh Sleep Quality Index in cancer patients. J Pain Symptom Manag 27(2):140–148. https://doi.org/10.1016/j.jpainsymman.2003.12.002
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 Manag 33(4):398–409. https://doi.org/10.1016/j.jpainsymman.2006.09.022
Miaskowski C, Cooper BA, Paul SM, Dodd M, Lee K, Aouizerat BE, West C, Cho M, Bank A (2006) Subgroups of patients with cancer with different symptom experiences and quality-of-life outcomes: a cluster analysis. Oncol Nurs Forum 33(5):E79–E89. https://doi.org/10.1188/06.ONF.E79-E89
Aizer AA, Chen M-H, McCarthy EP et al (2013) Marital status and survival in patients with cancer. J Clin Oncol 31(31):3869–3876. https://doi.org/10.1200/JCO.2013.49.6489
Meeske K, Smith AW, Alfano CM, McGregor BA, McTiernan A, Baumgartner KB, Malone KE, Reeve BB, Ballard-Barbash R, Bernstein L (2007) Fatigue in breast cancer survivors two to five years post diagnosis: a HEAL Study report. Qual Life Res 16(6):947–960. https://doi.org/10.1007/s11136-007-9215-3
Hwang SS, Chang VT, Rue M, Kasimis B (2003) Multidimensional independent predictors of cancer-related fatigue. J Pain Symptom Manag 26(1):604–614
Onen SH, Onen F, Courpron P, Dubray C (2005) How pain and analgesics disturb sleep. Clin J Pain 21(5):422–431
Foley D, Ancoli-Israel S, Britz P, Walsh J (2004) Sleep disturbances and chronic disease in older adults: results of the 2003 National Sleep Foundation Sleep in America Survey. J Psychosom Res 56(5):497–502. https://doi.org/10.1016/j.jpsychores.2004.02.010
Acknowledgments
The authors would like to thank Dr. Lianqi Liu for his contributions to this study and all patients for their time and participation.
Funding
Funding for this research was provided by the National Cancer Institute (grant numbers CA112035 and UL1RR03198), the National Institutes of Health (grant number M01 RR00827), the Stein Institute for Research on Aging, and the Department of Veterans Affairs Center of Excellence for Stress and Mental Health.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Sonia Ancoli-Israel consults for Merck, Eisai, Purdue, and Pfizer. All other authors have no conflicts of interest to disclose. The authors have full control of all primary data and agree to allow the journal to review these data if requested.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Fox, R.S., Ancoli-Israel, S., Roesch, S.C. et al. Sleep disturbance and cancer-related fatigue symptom cluster in breast cancer patients undergoing chemotherapy. Support Care Cancer 28, 845–855 (2020). https://doi.org/10.1007/s00520-019-04834-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00520-019-04834-w