Skip to main content

Advertisement

SpringerLink
Log in

Subgroups of patients undergoing chemotherapy with distinct cognitive fatigue and evening physical fatigue profiles

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

Abstract

Purpose

The purpose was to model cognitive fatigue and evening physical fatigue together to determine subgroups of patients with distinct cognitive fatigue AND evening physical fatigue profiles. Once these profiles were identified, differences among the subgroups in demographic and clinical characteristics, co-occurring symptoms, and quality of life outcomes were evaluated.

Methods

Oncology patients (n = 1332) completed self-report measures of cognitive fatigue and evening physical fatigue, six times over two cycles of chemotherapy. Latent profile analysis, which combined the two symptom scores, was done to identify subgroups of patients with distinct cognitive fatigue AND evening physical fatigue profiles.

Results

Three distinct profiles (i.e., Low [20.5%], Moderate [39.6%], and High [39.6%]) were identified. Compared to the Low class, patients in the High class were younger, female, and more likely to live alone and had a higher comorbidity burden and a lower functional status. In addition, these patients had a higher symptom burden and a poorer quality of life.

Conclusion

Based on clinically meaningful cutoff scores, 80% of the patients in this study had moderate to high levels of both cognitive fatigue and evening physical fatigue. In addition, these patients experienced high levels of other common symptoms (e.g., anxiety, depression, sleep disturbance, and pain). These co-occurring symptoms and other modifiable characteristics associated with membership in the Moderate and High classes may be potential targets for individualized symptom management interventions.

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. Abrahams HJG, Gielissen MFM, Verhagen C, 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

    CAS  PubMed  Google Scholar 

  2. Adams RN, Mosher CE, Winger JG, Abonour R, Kroenke K (2018) Cancer-related loneliness mediates the relationships between social constraints and symptoms among cancer patients. J Behav Med 41:243–252

    PubMed  Google Scholar 

  3. Al Maqbali M, Al Sinani M, Al Naamani Z, Al Badi K, Tanash MI (2021) Prevalence of fatigue in patients with cancer: a systematic review and meta-analysis. J Pain Symptom Manage 61:167–189

    PubMed  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

    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

    Google Scholar 

  6. 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 n (2015) Cancer-Related Fatigue, Version 2.2015. J Natl Compr Cancer Netw 13:1012–1039

    Google Scholar 

  7. Bower JE (2019) The role of neuro-immune interactions in cancer-related fatigue: biobehavioral risk factors and mechanisms. Cancer 125:353–364

    PubMed  Google Scholar 

  8. Chen YJ, Li XX, Ma HK, Zhang X, Wang BW, Guo TT, Xiao Y, Bing ZT, Ge L, Yang KH, Han XM (2020) Exercise training for improving patient-reported outcomes in patients with advanced-stage cancer: a systematic review and meta-analysis. J Pain Symptom Manage 59:734-749.e710

    PubMed  Google Scholar 

  9. 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

    PubMed  Google Scholar 

  10. Cimprich B, Visovatti M, Ronis DL (2011) The Attentional Function Index-a self-report cognitive measure. Psychooncology 20:194–202

    PubMed  Google Scholar 

  11. 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

    PubMed  Google Scholar 

  12. de Jong N, Candel MJ, Schouten HC, Abu-Saad HH, Courtens AM (2004) Prevalence and course of fatigue in breast cancer patients receiving adjuvant chemotherapy. Ann Oncol 15:896–905

    PubMed  Google Scholar 

  13. de Jong N, Candel MJ, Schouten HC, Abu-Saad HH, Courtens AM (2005) Course of mental fatigue and motivation in breast cancer patients receiving adjuvant chemotherapy. Ann Oncol 16:372–382

    PubMed  Google Scholar 

  14. de Jong N, Kester AD, Schouten HC, Abu-Saad HH, Courtens AM (2006) Course of fatigue between two cycles of adjuvant chemotherapy in breast cancer patients. Cancer Nurs 29:467–477

    PubMed  Google Scholar 

  15. de Raaf PJ, de Klerk C, van der Rijt CC (2013) Elucidating the behavior of physical fatigue and mental fatigue in cancer patients: a review of the literature. Psychooncology 22:1919–1929

    PubMed  Google Scholar 

  16. Dew IT, Buchler N, Dobbins IG, Cabeza R (2012) Where is ELSA? The early to late shift in aging. Cereb Cortex 22:2542–2553

    PubMed  Google Scholar 

  17. Dimsdale JE, Ancoli-Israel S, Ayalon L, Elsmore TF, Gruen W (2007) Taking fatigue seriously, II: variability in fatigue levels in cancer patients. Psychosomatics 48:247–252

    PubMed  Google Scholar 

  18. Dupont A, Bower JE, Stanton AL, Ganz PA (2014) Cancer-related intrusive thoughts predict behavioral symptoms following breast cancer treatment. Health Psychol 33:155–163

    PubMed  Google Scholar 

  19. 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. Eur J Cancer 40:1193–1198

    CAS  PubMed  Google Scholar 

  20. 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

    PubMed  Google Scholar 

  21. Gupta D, Lis CG, Grutsch JF (2007) The relationship between cancer-related fatigue and patient satisfaction with quality of life in cancer. J Pain Symptom Manage 34:40–47

    PubMed  Google Scholar 

  22. Hamidou Z, Dabakuyo TS, Bonnetain F (2011) Impact of response shift on longitudinal quality-of-life assessment in cancer clinical trials. Expert Rev Pharmacoecon Outcomes Res 11:549–559

    PubMed  Google Scholar 

  23. Han Tatiana J, Felger Jennifer C, Lee Anna, Mister Donna, Miller Andrew H, Torres Mylin A (2016) Association of childhood trauma with fatigue, depression, stress, and inflammation in breast cancer patients undergoing radiotherapy. Psychooncology 25:187–193

    PubMed  Google Scholar 

  24. Henry DH, Viswanathan HN, Elkin EP, Traina S, Wade S, Cella D (2008) Symptoms and treatment burden associated with cancer treatment: results from a cross-sectional national survey in the U.S. Support Care Cancer 16:791–801

    PubMed  Google Scholar 

  25. Huehnchen P, van Kampen A, Boehmerle W, Endres M (2020) Cognitive impairment after cytotoxic chemotherapy. Neurooncol Pract 7:11–21

    PubMed  Google Scholar 

  26. Hughes A, Suleman S, Rimes KA, Marsden J, Chalder T (2020) Cancer-related fatigue and functional impairment—towards an understanding of cognitive and behavioural factors. J Psychosom Res 134:110127

    PubMed  Google Scholar 

  27. Institute of Medicine (2012) Living well with chronic illness: a call for public health sction. In: Living Well with Chronic Illness: A Call for Public Health Action. The National Academies Press, Washington, DC

  28. Jacobs JM, Ream ME, Pensak N, Nisotel LE, Fishbein JN, MacDonald JJ, Buzaglo J, Lennes IT, Safren SA, Pirl WF, Temel JS, Greer JA (2019) Patient experiences with oral chemotherapy: adherence, symptoms, and quality of life. J Natl Compr Cancer Netw 17:221–228

    Google Scholar 

  29. Jung JY, Lee JM, Kim MS, Shim YM, Zo JI, Yun YH (2018) Comparison of fatigue, depression, and anxiety as factors affecting posttreatment health-related quality of life in lung cancer survivors. Psychooncology 27:465–470

    PubMed  Google Scholar 

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

    Google Scholar 

  31. Karnofsky D (1977) Performance scale. Plenum Press, New York

    Google Scholar 

  32. Kessels E, Husson O, van der Feltz-Cornelis CM (2018) The effect of exercise on cancer-related fatigue in cancer survivors: a systematic review and meta-analysis. Neuropsychiatr Dis Treat 14:479–494

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Kim HJ, Barsevick AM, Fang CY, Miaskowski C (2012) Common biological pathways underlying the psychoneurological symptom cluster in cancer patients. Cancer Nurs 35:E1–E20

    PubMed  Google Scholar 

  34. Kuhlman KR, Chiang JJ, Horn S, Bower JE (2017) Developmental psychoneuroendocrine and psychoneuroimmune pathways from childhood adversity to disease. Neurosci Biobehav Rev 80:166–184

    CAS  PubMed  PubMed Central  Google Scholar 

  35. 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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  38. 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. Psychooncology 18:187–194

    PubMed  PubMed Central  Google Scholar 

  39. Matura LA, Malone S, Jaime-Lara R, Riegel B (2018) A systematic review of biological mechanisms of fatigue in chronic illness. Biol Res Nurs 20:410–421

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 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 26(3):e12437. https://doi.org/10.1111/ecc.12437

    Article  Google Scholar 

  41. 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

    PubMed  Google Scholar 

  42. Mustian KM, Alfano CM, Heckler C, Kleckner AS, Kleckner IR, Leach CR, Mohr D, Palesh OG, Peppone LJ, Piper BF, Scarpato J, Smith T, Sprod LK, Miller SM (2017) Comparison of pharmaceutical, psychological, and exercise treatments for cancer-related fatigue: a meta-analysis. JAMA Oncol 3:961–968

    PubMed  PubMed Central  Google Scholar 

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

  44. Nguyen TT, Lee EE, Daly RE, Wu TC, Tang Y, Tu X, Van Patten R, Jeste DV, Palmer BW (2020) Predictors of loneliness by age decade: study of psychological and environmental factors in 2,843 community-dwelling Americans aged 20–69 years. J Clin Psychiatry 81

  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

    CAS  PubMed  Google Scholar 

  46. Pertl MM, Hevey D, Collier S, Lambe K, O’Dwyer AM (2014) Predictors of fatigue in cancer patients before and after chemotherapy. J Health Psychol 19:699–710

    PubMed  Google Scholar 

  47. Puigpinos-Riera R, Serral G, Sala M, Bargallo X, Quintana MJ, Espinosa M, Manzanera R, Domenech M, Macia F, Grau J, Vidal E (2020) Cancer-related fatigue and its determinants in a cohort of women with breast cancer: the DAMA Cohort. Support Care Cancer 28:5213–5221

    CAS  PubMed  Google Scholar 

  48. Radbruch L, Strasser F, Elsner F, Gonçalves JF, Løge J, Kaasa S, Nauck F, Stone P (2008) Fatigue in palliative care patients — an EAPC approach. Palliat Med 22:13–32

    PubMed  Google Scholar 

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

    Google Scholar 

  50. Rau KM, Shun SC, Chiou TJ, Lu CH, Ko WH, Lee MY, Huang WT, Yeh KH, Chang CS, Hsieh RK (2020) A nationwide survey of fatigue in cancer patients in Taiwan: an unmet need. Jpn J Clin Oncol 50:693–700

    PubMed  PubMed Central  Google Scholar 

  51. 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

    PubMed  Google Scholar 

  52. Schmidt ME, Hermann S, Arndt V, Steindorf K (2020) Prevalence and severity of long‐term physical, emotional, and cognitive fatigue across 15 different cancer entities. Cancer Med 9:8053–8061

    PubMed  PubMed Central  Google Scholar 

  53. Schmidt ME, Wiskemann J, Schneeweiss A, Potthoff K, Ulrich CM, Steindorf K (2018) Determinants of physical, affective, and cognitive fatigue during breast cancer therapy and 12 months follow-up. Int J Cancer 142:1148–1157

    CAS  PubMed  Google Scholar 

  54. Singer S, Kuhnt S, Zwerenz R, Eckert K, Hofmeister D, Dietz A, Giesinger J, Hauss J, Papsdorf K, Briest S, Brown A (2011) Age- and sex-standardised prevalence rates of fatigue in a large hospital-based sample of cancer patients. Br J Cancer 105:445–451

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Smets EM, Garssen B, Bonke B, De Haes JC (1995) The Multidimensional Fatigue Inventory (MFI) psychometric qualities of an instrument to assess fatigue. J Psychosom Res 39:315–325

    CAS  PubMed  Google Scholar 

  56. 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

    Google Scholar 

  57. Stein KD, Martin SC, Hann DM, Jacobsen PB (1998) A multidimensional measure of fatigue for use with cancer patients. Cancer Pract 6:143–152

    CAS  PubMed  Google Scholar 

  58. Thong MSY, Mols F, van de Poll-Franse LV, Sprangers MAG, van der Rijt CCD, Barsevick AM, Knoop H, Husson O (2018) Identifying the subtypes of cancer-related fatigue: results from the population-based PROFILES registry. J Cancer Surviv 12:38–46

    PubMed  Google Scholar 

  59. Tsaras K, Papathanasiou IV, Mitsi D, Veneti A, Kelesi M, Zyga S, Fradelos EC (2018) Assessment of depression and anxiety in breast cancer patients: prevalence and associated factors. Asian Pac J Cancer Prev 19:1661–1669

    PubMed  PubMed Central  Google Scholar 

  60. Ware J, 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

    PubMed  Google Scholar 

  61. Wildiers H, Heeren P, Puts M, Topinkova E, Janssen-Heijnen ML, Extermann M, Falandry C, Artz A, Brain E, Colloca G, Flamaing J, Karnakis T, Kenis C, Audisio RA, Mohile S, Repetto L, Van Leeuwen B, Milisen K, Hurria A (2014) International Society of Geriatric Oncology consensus on geriatric assessment in older patients with cancer. J Clin Oncol 32:2595–2603

    PubMed  PubMed Central  Google Scholar 

  62. Williams AM, Khan CP, Heckler CE, Barton DL, Ontko M, Geer J, Kleckner AS, Dakhil S, Mitchell J, Mustian KM, Peppone LJ, Kipnis V, Kamen CS, O’Mara AM, Janelsins MC (2021) Fatigue, anxiety, and quality of life in breast cancer patients compared to non-cancer controls: a nationwide longitudinal analysis. Breast Cancer Res Treat 187(1):275–285. https://doi.org/10.1007/s10549-020-06067-6

    Article  CAS  PubMed  Google Scholar 

  63. Witek Janusek L, Tell D, Albuquerque K, Mathews HL (2013) Childhood adversity increases vulnerability for behavioral symptoms and immune dysregulation in women with breast cancer. Brain Behav Immun 30 Suppl:S149-162

    PubMed  Google Scholar 

  64. Wright F, Cooper BA, Conley YP, Hammer MJ, Chen LM, Paul SM, Levine JD, Miaskowski C, Kober KM (2017) Distinct evening fatigue profiles in oncology outpatients receiving chemotherapy Fatigue. Biomed Health Behav 5:131–144

    Google Scholar 

  65. Wright F, D’Eramo Melkus G, Hammer M, Schmidt BL, Knobf MT, Paul SM, Cartwright F, Mastick J, Cooper BA, Chen LM, Melisko M, Levine JD, Kober K, Aouizerat BE, Miaskowski C (2015) Predictors and trajectories of morning fatigue are distinct from evening fatigue. J Pain Symptom Manage 50:176–189

    PubMed  PubMed Central  Google Scholar 

  66. Wright F, D’Eramo Melkus G, Hammer M, Schmidt BL, Knobf MT, Paul SM, Cartwright F, Mastick J, Cooper BA, Chen LM, Melisko M, Levine JD, Kober K, Aouizerat BE, Miaskowski C (2015) Trajectories of evening fatigue in oncology outpatients receiving chemotherapy. J Pain Symptom Manage 50:163–175

    PubMed  PubMed Central  Google Scholar 

  67. Wright F, Dunn LB, Paul SM, Conley YP, Levine JD, Hammer MJ, Cooper BA, Miaskowski C, Kober KM (2019) Morning fatigue severity profiles in oncology outpatients receiving chemotherapy. Cancer Nurs 42:355–364

    PubMed  PubMed Central  Google Scholar 

  68. Wright F, Hammer M, Paul SM, Aouizerat BE, Kober KM, Conley YP, Cooper BA, Dunn LB, Levine JD, Dem G, Miaskowski C (2017) Inflammatory pathway genes associated with inter-individual variability in the trajectories of morning and evening fatigue in patients receiving chemotherapy. Cytokine 91:187–210

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Wright F, Hammer MJ, D’Eramo Melkus G (2014) Associations between multiple chronic conditions and cancer-related fatigue: an integrative review. Oncol Nurs Forum 41:399–410

    PubMed  Google Scholar 

Download references

Funding

This study was funded by a grant from the National Cancer Institute (CA134900). Dr. Miaskowski is an American Cancer Society Clinical Research Professor.

Author information

Authors and Affiliations

  1. Department of Physiological Nursing, University of California, 2 Koret Way – N631Y, San Francisco, CA, 94143-0610, USA

    Lisa Morse, Kord M. Kober, Carol Viele, Bruce A. Cooper, Steven M. Paul & Christine Miaskowski

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

    Yvette P. Conley

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

    Marilyn Hammer

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

    Jon D. Levine

Authors
  1. Lisa Morse
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kord M. Kober
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carol Viele
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bruce A. Cooper
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Steven M. Paul
    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 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 and 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

This study was exempted from written informed consent.

Consent for publication

All of the authors approved the final paper for publication.

Conflict of interest

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

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morse, L., Kober, K.M., Viele, C. et al. Subgroups of patients undergoing chemotherapy with distinct cognitive fatigue and evening physical fatigue profiles. Support Care Cancer 29, 7985–7998 (2021). https://doi.org/10.1007/s00520-021-06410-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00520-021-06410-7

Keywords

Search

Navigation