Skip to main content
SpringerLink
Log in

Distinct sleep disturbance and cognitive dysfunction profiles in oncology outpatients receiving chemotherapy

  • Original Article
  • Published:
Supportive Care in Cancer Aims and scope Submit manuscript

Abstract

Purpose

Sleep disturbance and cancer-related cognitive impairment (CRCI) are two of the most common symptoms reported by patients undergoing chemotherapy. Less is known about how these symptoms co-occur and their associated risk factors. Study purposes were to identify subgroups of patients with distinct sleep disturbance and CRCI profiles and evaluate for differences among the subgroups in demographic and clinical characteristics, symptom severity scores, and QOL outcomes.

Methods

A total of 1,333 oncology outpatients receiving chemotherapy completed self-report questionnaires on sleep disturbance and cognitive dysfunction six times over two cycles of chemotherapy. Latent profile analysis was used to identify distinct sleep disturbance AND cognitive dysfunction profiles. Parametric and non-parametric tests were used to evaluate for differences among the classes.

Results

Two distinct profiles were identified (i.e., Low = low levels of both sleep disturbance and cognitive dysfunction (53.5%); High = high levels of both sleep disturbance and cognitive dysfunction (45.5%)). Patients in the High class were younger, more likely to be female, had a lower functional status and a higher level of comorbidity. In addition, these patients had a higher symptom burden and a lower quality of life.

Conclusion

Almost half of the patients undergoing chemotherapy experienced clinically meaningful levels of both symptoms. Of note, sleep disturbance is frequently overlooked by both clinicians and patients. Clinicians need to recommend cognitive rehabilitation and physical activity programs to decrease patients’ symptom burden.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Data availability

Data will be provided to the publisher after they obtain a material transfer agreement from the University of California, San Francisco.

References

  1. Acker KA, Carter P (2021) Sleep-wake disturbances in oncology. Nurs Clin North Am 56:175–187

    Article  PubMed  Google Scholar 

  2. Ahles TA, Root JC (2018) Cognitive effects of cancer and cancer treatments. Annu Rev Clin Psychol 14:425–451

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Atallah M, Cooper B, Munoz RF, Paul SM, Anguera J, Levine JD, Hammer M, Wright F, Chen LM, Melisko M, Conley YP, Miaskowski C, Dunn LB (2020) Psychological symptoms and stress are associated with decrements in attentional function in cancer patients undergoing chemotherapy. Cancer Nurs 43:402–410

    Article  PubMed  Google Scholar 

  5. Babor TF, Higgins-Biddle JC, Saunders JB, Monteiro MG (2001) AUDIT: the alcohol use disorders identification test: guidelines for use in primary care. World Health Organization, Geneva, Switzerland

    Google Scholar 

  6. Cimprich B (1992) Attentional fatigue following breast cancer surgery. Res Nurs Health 15:199–207

    Article  CAS  PubMed  Google Scholar 

  7. Cimprich B, So H, Ronis DL, Trask C (2005) Pre-treatment factors related to cognitive functioning in women newly diagnosed with breast cancer. Psychooncology 14:70–78

    Article  PubMed  Google Scholar 

  8. Cimprich B, Visovatti M, Ronis DL (2011) The attentional function index–a self-report cognitive measure. Psychooncology 20:194–202

    Article  PubMed  Google Scholar 

  9. Daut RL, Cleeland CS, Flanery RC (1983) Development of the Wisconsin brief pain questionnaire to assess pain in cancer and other diseases. Pain 17:197–210

    Article  PubMed  Google Scholar 

  10. Dolsen MR, Crosswell AD, Prather AA (2019) Links between stress, sleep, and inflammation: are there sex differences? Curr Psychiatry Rep 21:8

    Article  PubMed  PubMed Central  Google Scholar 

  11. Duivon M, Giffard B, Desgranges B, Perrier J (2021) Are sleep complaints related to cognitive functioning in non-central nervous system cancer? A systematic review Neuropsychol Rev

  12. Extermann M, Bonetti M, Sledge GW, O’Dwyer PJ, Bonomi P, Benson AB 3rd (2004) MAX2–a convenient index to estimate the average per patient risk for chemotherapy toxicity; validation in ECOG trials. European J Cancer 40:1193–1198

    Article  CAS  Google Scholar 

  13. Fang YY, Hung CT, Chan JC, Huang SM, Lee YH (2019) Meta-analysis: exercise intervention for sleep problems in cancer patients. Eur J Cancer Care (Engl) 28:e13131

    Article  Google Scholar 

  14. Fletcher BS, Paul SM, Dodd MJ, Schumacher K, West C, Cooper B, Lee K, Aouizerat B, Swift P, Wara W, Miaskowski CA (2008) Prevalence, severity, and impact of symptoms on female family caregivers of patients at the initiation of radiation therapy for prostate cancer. J Clin Oncol 26:599–605

    Article  PubMed  Google Scholar 

  15. Garland SN, Ivers H, Savard J (2021) Prospective rates, longitudinal associations, and factors associated with comorbid insomnia symptoms and perceived cognitive impairment. Front Neurosci 15:817933

    Article  PubMed  Google Scholar 

  16. Gay CL, Lee KA, Lee SY (2004) Sleep patterns and fatigue in new mothers and fathers. Biol Res Nurs 5:311–318

    Article  PubMed  Google Scholar 

  17. Gibson EM, Monje M (2019) Emerging mechanistic underpinnings and therapeutic targets for chemotherapy-related cognitive impairment. Curr Opin Oncol 31:531–539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Henneghan A (2016) Modifiable factors and cognitive dysfunction in breast cancer survivors: a mixed-method systematic review. Support Care Cancer 24:481–497

    Article  PubMed  Google Scholar 

  19. Henneghan A, Haley AP, Kesler S (2020) Exploring relationships among peripheral amyloid beta, tau, cytokines, cognitive function, and psychosomatic symptoms in breast cancer survivors. Biol Res Nurs 22:126–138

    Article  CAS  PubMed  Google Scholar 

  20. Howell D, Oliver TK, Keller-Olaman S, Davidson JR, Garland S, Samuels C, Savard J, Harris C, Aubin M, Olson K, Sussman J, MacFarlane J, Taylor C (2014) Sleep disturbance in adults with cancer: a systematic review of evidence for best practices in assessment and management for clinical practice. Ann Oncol 25:791–800

    Article  CAS  PubMed  Google Scholar 

  21. Hu M, Zhang P, Li C, Tan Y, Li G, Xu D, Chen L (2017) Sleep disturbance in mild cognitive impairment: a systematic review of objective measures. Neurol Sci 38:1363–1371

    Article  PubMed  Google Scholar 

  22. Huang BH, Duncan MJ, Cistulli PA, Nassar N, Hamer M, Stamatakis E (2021) Sleep and physical activity in relation to all-cause, cardiovascular disease and cancer mortality risk Br J Sports Med

  23. Innominato PF, Spiegel D, Ulusakarya A, Giacchetti S, Bjarnason GA, Lévi F, Palesh O (2015) Subjective sleep and overall survival in chemotherapy-naïve patients with metastatic colorectal cancer. Sleep Med 16:391–398

    Article  PubMed  Google Scholar 

  24. Jakovljevic K, Kober KM, Block A, Cooper BA, Paul SM, Hammer MJ, Cartwright F, Conley YP, Wright F, Dunn LB, Levine JD, Miaskowski C (2021) Higher levels of stress are associated with a significant symptom burden in oncology outpatients receiving chemotherapy. J Pain Symptom Manage 61(24–31):e24

    Article  Google Scholar 

  25. Jung T, Wickrama KAS (2008) An introduction to latent class growth analysis and growth mixture modeling Soc Pers Psychol. Compass 2:302–317

    Google Scholar 

  26. Karnofsky D, Abelmann WH, Craver LV, Burchenal JH (1948) The use of nitrogen mustards in the palliative treatment of carcinoma. Cancer 1:634–656

    Article  Google Scholar 

  27. Lange M, Joly F, Vardy J, Ahles T, Dubois M, Tron L, Winocur G, De Ruiter MB, Castel H (2019) Cancer-related cognitive impairment: an update on state of the art, detection, and management strategies in cancer survivors. Ann Oncol 30:1925–1940

    Article  CAS  PubMed  Google Scholar 

  28. Langford DJ, Cooper B, Paul S, Humphreys J, Hammer MJ, Levine J, Conley YP, Wright F, Dunn LB, Miaskowski C (2020) Distinct stress profiles among oncology patients undergoing chemotherapy. J Pain Symptom Manage 59:646–657

    Article  PubMed  Google Scholar 

  29. Lee KA (1992) Self-reported sleep disturbances in employed women. Sleep 15:493–498

    Article  CAS  PubMed  Google Scholar 

  30. Lee KA, Hicks G, Nino-Murcia G (1991) Validity and reliability of a scale to assess fatigue. Psychiatry Res 36:291–298

    Article  CAS  PubMed  Google Scholar 

  31. Liou KT, Ahles TA, Garland SN, Li QS, Bao T, Li Y, Root JC, Mao JJ (2019) The relationship between insomnia and cognitive impairment in breast cancer survivors. JNCI Cancer Spectr 3:pkz041

    Article  PubMed  PubMed Central  Google Scholar 

  32. Loh KP, Janelsins MC, Mohile SG, Holmes HM, Hsu T, Inouye SK, Karuturi MS, Kimmick GG, Lichtman SM, Magnuson A, Whitehead MI, Wong ML, Ahles TA (2016) Chemotherapy-related cognitive impairment in older patients with cancer J Geriatr. Oncol 7:270–280

    Google Scholar 

  33. Loh KP, Pandya C, Zittel J, Kadambi S, Flannery M, Reizine N, Magnuson A, Braganza G, Mustian K, Dale W, Duberstein P, Mohile SG (2017) Associations of sleep disturbance with physical function and cognition in older adults with cancer. Support Care Cancer 25:3161–3169

    Article  PubMed  PubMed Central  Google Scholar 

  34. McCall MK, Connolly M, Nugent B, Conley YP, Bender CM, Rosenzweig MQ (2020) Symptom experience, management, and outcomes according to race and social determinants including genomics, epigenomics, and metabolomics (SEMOARS + GEM): an explanatory model for breast cancer treatment disparity. J Cancer Educ 35:428–440

    Article  PubMed  Google Scholar 

  35. Miaskowski C, Cooper BA, Aouizerat B, Melisko M, Chen LM, Dunn L, Hu X, Kober KM, Mastick J, Levine JD, Hammer M, Wright F, Harris J, Armes J, Furlong E, Fox P, Ream E, Maguire R, Kearney N (2017) The symptom phenotype of oncology outpatients remains relatively stable from prior to through 1 week following chemotherapy. Eur J Cancer Care (Engl) 26(10):111

    Google Scholar 

  36. 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 120:2371–2378

    Article  PubMed  Google Scholar 

  37. Mravec B, Tibensky M, Horvathova L (2020) Stress and cancer Part I: Mechanisms mediating the effect of stressors on cancer. J Neuroimmunol 346:577311–577311

    Article  CAS  PubMed  Google Scholar 

  38. Muthen B, Shedden K (1999) Finite mixture modeling with mixture outcomes using the EM algorithm. Biometrics 55:463–469

    Article  CAS  PubMed  Google Scholar 

  39. Muthen BO (2001) Latent variable mixture modeling. In: Marcoulides GA, Schumacher RE (eds) New developments and techniques in structural equation modeling. Lawrence Erlbaum Associates, Mahwah, NJ

    Google Scholar 

  40. Muthen BO (2002) Beyond SEM: General latent variable modeling. Behaviormetrika 29:81–117

    Article  Google Scholar 

  41. Muthen BO (2004) Latent variable analysis: growth mixture modeling and related techniques for longitudinal data. In: Kaplan DW (ed) Handbook of Quantitative Methodology for the Social Sciences. Sage Publications, Newbury Park, CA, pp 345–368

    Google Scholar 

  42. Muthén L, Muthén B (2009) Mplus statistical analysis with latent variables: user’s guide 7

  43. Muthen LK, Muthen BO (1998-2020) Mplus user’s guide (8th ed). Muthen & Muthen, Los Angeles, CA

  44. Országhová Z, Mego M, Chovanec M (2021) Long-term cognitive dysfunction in cancer survivors. Front Mol Biosci 8:770413

    Article  PubMed  PubMed Central  Google Scholar 

  45. Padilla GV, Ferrell B, Grant MM, Rhiner M (1990) Defining the content domain of quality of life for cancer patients with pain. Cancer Nurs 13:108–115

    Article  CAS  PubMed  Google Scholar 

  46. 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 28:292–298

    Article  PubMed  Google Scholar 

  47. Park JH, Bae SH, Jung YS, Jung YM (2015) Prevalence and characteristics of chemotherapy-related cognitive impairment in patients with breast cancer. J Korean Acad Nurs 45:118–128

    Article  PubMed  Google Scholar 

  48. Radloff LS (1977) The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas 1:385–401

    Article  Google Scholar 

  49. Rodriguez N, Fawcett JM, Rash JA, Lester R, Powell E, MacMillan CD, Garland SN (2021) Factors associated with cognitive impairment during the first year of treatment for nonmetastatic breast cancer. Cancer Med 10:1191–1200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Sangha O, Stucki G, Liang MH, Fossel AH, Katz JN (2003) The self-administered comorbidity questionnaire: a new method to assess comorbidity for clinical and health services research. Arthritis Rheum 49:156–163

    Article  PubMed  Google Scholar 

  51. 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 121:1703–1711

    Article  PubMed  Google Scholar 

  52. Scheff NN, Saloman JL (2021) Neuroimmunology of cancer and associated symptomology. Immunol Cell Biol 99:949–961

    Article  PubMed  PubMed Central  Google Scholar 

  53. So WKW, Law BMH, Chan DNS, Xing W, Chan CWH, McCarthy AL (2020) The effect of nonpharmacological interventions on managing symptom clusters among cancer patients: a systematic review. Cancer Nurs 43:E304-e327

    Article  PubMed  Google Scholar 

  54. Souza R, Dos Santos MR (2020) das Chagas Valota IA, Sousa CS, Costa Calache ALS Factors associated with sleep quality during chemotherapy: an integrative review. Nurs Open 7:1274–1284

    Article  PubMed  PubMed Central  Google Scholar 

  55. Spielberger CG, Gorsuch RL, Suchene R, Vagg PR, Jacobs GA (1983) Manual for the state-anxiety (Form Y): self evaluation questionnaire. Consulting Psychologists Press, Palo Alto, CA

    Google Scholar 

  56. Substance Use and Mental Health Services Administration (2016) Impact of the DSM-IV to DSM-5 changes on the national survey on drug use and health. In: Impact of the DSM-IV to DSM-5 Changes on the National Survey on Drug Use and Health. Substance Abuse and Mental Health Services Administration. https://www.ncbi.nlm.nih.gov/books/NBK519704/table/ch3.t36/. Accessed 15 Mar 2022

  57. Tejada M, Viele C, Kober KM, Cooper BA, Paul SM, Dunn LB, Hammer MJ, Wright F, Conley YP, Levine JD, Miaskowski C (2019) Identification of subgroups of chemotherapy patients with distinct sleep disturbance profiles and associated co-occurring symptoms Sleep 42

  58. Vega JN, Dumas J, Newhouse PA (2017) Cognitive effects of chemotherapy and cancer-related treatments in older adults. Am J Geriatr Psychiatry 25:1415–1426

    Article  PubMed  PubMed Central  Google Scholar 

  59. Vitali M, Ripamonti CI, Roila F, Proto C, Signorelli D, Imbimbo M, Corrao G, Brissa A, Rosaria G, de Braud F, Garassino MC, Lo Russo G (2017) Cognitive impairment and chemotherapy: a brief overview. Crit Rev Oncol Hematol 118:7–14

    Article  PubMed  Google Scholar 

  60. Ware J Jr, Kosinski M, Keller SD (1996) A 12-item short-form health survey: construction of scales and preliminary tests of reliability and validity. Med Care 34:220–233

    Article  PubMed  Google Scholar 

Download references

Funding

This study was funded by a grant from the National Cancer Institute (CA134900). Ms. Huang was partially funded by the American Cancer Society, the William and Jacquelyn Tobias Foundation, and the San Francisco Bay Area Oncology Nursing Society. Dr. Miaskowski is an American Cancer Society Clinical Research Professor.

Author information

Authors and Affiliations

  1. School of Nursing, University of California, 2 Koret Way - Box 0610, San Francisco, CA, 94143-0610, USA

    Vivian Huang, Lynda Mackin, Kord M. Kober, Steven M. Paul, Bruce A. Cooper & Christine Miaskowski

  2. School of Nursing, University of Pittsburgh, Pittsburgh, PA, USA

    Yvette P. Conley

  3. Dana Farber Cancer Institute, Boston, MA, USA

    Marilyn J. Hammer

  4. School of Medicine, University of California, San Francisco, CA, USA

    Jon D. Levine & Christine Miaskowski

Authors
  1. Vivian Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lynda Mackin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kord M. Kober
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Steven M. Paul
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bruce A. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yvette P. Conley
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marilyn J. Hammer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jon D. Levine
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Christine Miaskowski
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All of the authors participated in the revisions to this paper, the interpretation of the results, and approved the final paper.

Corresponding author

Correspondence to Christine Miaskowski.

Ethics declarations

Ethics approval

This study was approved by the Committee on Human Research at the University of California.

Consent to participate

All patients signed written informed consent to participate in this study.

Consent for publication

All of the authors approved the final paper for publication.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, V., Mackin, L., Kober, K.M. et al. Distinct sleep disturbance and cognitive dysfunction profiles in oncology outpatients receiving chemotherapy. Support Care Cancer 30, 9243–9254 (2022). https://doi.org/10.1007/s00520-022-07350-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00520-022-07350-6

Keywords

Search

Navigation