Cognitive Performance and Psychological Distress in Breast Cancer Patients at Disease Onset

Jochen Kaiser, Jörg Dietrich, Miena Amiri, Isa Rüschel, Hazal Akbaba, Nonda Hantke, Klaus Fliessbach, Bianca Senf, Christine Solbach, Christoph Bledowski, Jochen Kaiser, Jörg Dietrich, Miena Amiri, Isa Rüschel, Hazal Akbaba, Nonda Hantke, Klaus Fliessbach, Bianca Senf, Christine Solbach, Christoph Bledowski

Abstract

Objective: Many cancer patients complain about cognitive dysfunction. While cognitive deficits have been attributed to the side effects of chemotherapy, there is evidence for impairment at disease onset, prior to cancer-directed therapy. Further debated issues concern the relationship between self-reported complaints and objective test performance and the role of psychological distress.

Method: We assessed performance on neuropsychological tests of attention and memory and obtained estimates of subjective distress and quality of life in 27 breast cancer patients and 20 healthy controls. Testing in patients took place shortly after the initial diagnosis, but prior to subsequent therapy.

Results: While patients showed elevated distress, cognitive performance differed on a few subtests only. Patients showed slower processing speed and poorer verbal memory than controls. Objective and self-reported cognitive function were unrelated, and psychological distress correlated more strongly with subjective complaints than with neuropsychological test performance.

Conclusion: This study provides further evidence of limited cognitive deficits in cancer patients prior to the onset of adjuvant therapy. Self-reported cognitive deficits seem more closely related to psychological distress than to objective test performance.

Keywords: attention; breast cancer; cognitive functions; memory; psychological distress.

Copyright © 2019 Kaiser, Dietrich, Amiri, Rüschel, Akbaba, Hantke, Fliessbach, Senf, Solbach and Bledowski.

References

    1. Aaronson N. K., Ahmedzai S., Bergman B., Bullinger M., Cull A., Duez N. J., et al. (1993). The european organization for research and treatment of cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology. J. Natl. Cancer Inst. 85 365–376.
    1. Ahles T. A., Saykin A. J., McDonald B. C., Furstenberg C. T., Cole B. F., Hanscom B. S., et al. (2008). Cognitive function in breast cancer patients prior to adjuvant treatment. Breast Cancer Res. Treat 110 143–152. 10.1007/s10549-007-9686-5
    1. Ando-Tanabe N., Iwamitsu Y., Kuranami M., Okazaki S., Yasuda H., Nakatani Y., et al. (2014). Cognitive function in women with breast cancer receiving adjuvant chemotherapy and healthy controls. Breast Cancer 21 453–462. 10.1007/s12282-012-0405-7
    1. Andreotti C., Root J. C., Ahles T. A., McEwen B. S., Compas B. E. (2015). Cancer, coping, and cognition: a model for the role of stress reactivity in cancer-related cognitive decline. Psychooncology 24 617–623. 10.1002/pon.3683
    1. Arnsten A. F. (2015). Stress weakens prefrontal networks: molecular insults to higher cognition. Nat. Neurosci. 18 1376–1385. 10.1038/nn.4087
    1. Bender C. M., Sereika S. M., Berga S. L., Vogel V. G., Brufsky A. M., Paraska K. K., et al. (2006). Cognitive impairment associated with adjuvant therapy in breast cancer. Psychooncology 15 422–430.
    1. Biglia N., Bounous V. E., Malabaila A., Palmisano D., Torta D. M., D’Alonzo M., et al. (2012). Objective and self-reported cognitive dysfunction in breast cancer women treated with chemotherapy: a prospective study. Eur J Cancer Care 21 485–492. 10.1111/j.1365-2354.2011.01320.x
    1. Boykoff N., Moieni M., Subramanian S. K. (2009). Confronting chemobrain: an in-depth look at survivors’ reports of impact on work, social networks, and health care response. J. Cancer Surviv. 3 223–232. 10.1007/s11764-009-0098-x
    1. Cimprich B. (1992). Attentional fatigue following breast cancer surgery. Res. Nurs. Health 15 199–207. 10.1002/nur.4770150306
    1. Cimprich B., So H., Ronis D. L., Trask C. (2005). Pre-treatment factors related to cognitive functioning in women newly diagnosed with breast cancer. Psychooncology 14 70–78. 10.1002/pon.821
    1. Debess J., Riis J. O., Engebjerg M. C., Ewertz M. (2010). Cognitive function after adjuvant treatment for early breast cancer: a population-based longitudinal study. Breast Cancer Res. Treat 121 91–100. 10.1007/s10549-010-0756-8
    1. Debess J., Riis J. O., Pedersen L., Ewertz M. (2009). Cognitive function and quality of life after surgery for early breast cancer in North Jutland. Denmark. Acta Oncol. 48 532–540. 10.1080/02841860802600755
    1. Deprez S., Amant F., Yigit R., Porke K., Verhoeven J., Van den Stock J., et al. (2011). Chemotherapy-induced structural changes in cerebral white matter and its correlation with impaired cognitive functioning in breast cancer patients. Hum. Brain Mapp. 32 480–493. 10.1002/hbm.21033
    1. Deprez S., Billiet T., Sunaert S., Leemans A. (2013). Diffusion tensor MRI of chemotherapy-induced cognitive impairment in non-CNS cancer patients: a review. Brain Imaging Behav. 7 409–435. 10.1007/s11682-012-9220-1
    1. Dietrich J., Han R., Yang Y., Mayer-Proschel M., Noble M. (2006). CNS progenitor cells and oligodendrocytes are targets of chemotherapeutic agents in vitro and in vivo. J. Biol. 5:22. 10.1186/jbiol50
    1. Dietrich J., Monje M., Wefel J., Meyers C. (2008). Clinical patterns and biological correlates of cognitive dysfunction associated with cancer therapy. Oncologist 13 1285–1295. 10.1634/theoncologist.2008-0130
    1. Dietrich J., Prust M., Kaiser J. (2015). Chemotherapy, cognitive impairment and hippocampal toxicity. Neurosci 309 224–232. 10.1016/j.neuroscience.2015.06.016
    1. Fliessbach K., Hoppe C., Schlegel U., Elger C. E., Helmstaedter C. (2006). [NeuroCogFX–a computer-based neuropsychological assessment battery for the follow-up examination of neurological patients]. Fortschr. Neurol. Psychiatr. 74 643–650.
    1. Ganz P. A., Kwan L., Castellon S. A., Oppenheim A., Bower J. E., Silverman D. H., et al. (2013). Cognitive complaints after breast cancer treatments: examining the relationship with neuropsychological test performance. J. Natl. Cancer Inst. 105 791–801. 10.1093/jnci/djt073
    1. Hedayati E., Schedin A., Nyman H., Alinaghizadeh H., Albertsson M. (2011). The effects of breast cancer diagnosis and surgery on cognitive functions. Acta Oncol. 50 1027–1036. 10.3109/0284186X.2011.572911
    1. Hede K. (2008). Chemobrain is real but may need new name. J. Natl. Cancer Inst. 100:169.
    1. Hegel M. T., Moore C. P., Collins E. D., Kearing S., Gillock K. L., Riggs R. L., et al. (2006). Distress, psychiatric syndromes, and impairment of function in women with newly diagnosed breast cancer. Cancer 107 2924–2931. 10.1002/cncr.22335
    1. Hermelink K. (2015). Chemotherapy and cognitive function in breast cancer patients: the so-called chemo brain. J. Natl. Cancer Inst. Monogr. 2015 67–69. 10.1093/jncimonographs/lgv009
    1. Hermelink K., Buhner M., Sckopke P., Neufeld F., Kaste J., Voigt V., et al. (2017). Chemotherapy and post-traumatic stress in the causation of cognitive dysfunction in breast cancer patients. J. Natl. Cancer Inst. 109:djx057. 10.1093/jnci/djx057
    1. Hermelink K., Kuchenhoff H., Untch M., Bauerfeind I., Lux M. P., Buhner M., et al. (2010). Two different sides of ‘chemobrain’: determinants and nondeterminants of self-perceived cognitive dysfunction in a prospective, randomized, multicenter study. Psychooncology 19 1321–1328. 10.1002/pon.1695
    1. Hermelink K., Untch M., Lux M. P., Kreienberg R., Beck T., Bauerfeind I., et al. (2007). Cognitive function during neoadjuvant chemotherapy for breast cancer: results of a prospective, multicenter, longitudinal study. Cancer 109 1905–1913. 10.1002/cncr.22610
    1. Hermelink K., Voigt V., Kaste J., Neufeld F., Wuerstlein R., Buhner M., et al. (2015). Elucidating pretreatment cognitive impairment in breast cancer patients: the impact of cancer-related post-traumatic stress. J. Natl. Cancer Inst. 107:djw048. 10.1093/jnci/djw048
    1. Hutchinson A. D., Hosking J. R., Kichenadasse G., Mattiske J. K., Wilson C. (2012). Objective and subjective cognitive impairment following chemotherapy for cancer: a systematic review. Cancer Treat. Rev. 38 926–934. 10.1016/j.ctrv.2012.05.002
    1. Jansen C. E., Cooper B. A., Dodd M. J., Miaskowski C. A. (2011). A prospective longitudinal study of chemotherapy-induced cognitive changes in breast cancer patients. Support Care Cancer 19 1647–1656. 10.1007/s00520-010-0997-4
    1. Jenkins V., Shilling V., Deutsch G., Bloomfield D., Morris R., Allan S., et al. (2006). A 3-year prospective study of the effects of adjuvant treatments on cognition in women with early stage breast cancer. Br. J. Cancer 94 828–834. 10.1038/sj.bjc.6603029
    1. Johnson T., Monk T., Rasmussen L. S., Abildstrom H., Houx P., Korttila K., et al. (2002). Postoperative cognitive dysfunction in middle-aged patients. Anesthesiology 96 1351–1357. 10.1097/00000542-200206000-00014
    1. Kaiser J., Bledowski C., Dietrich J. (2014). Neural correlates of chemotherapy-related cognitive impairment. Cortex 54 33–50. 10.1016/j.cortex.2014.01.010
    1. Kuhlmann S., Piel M., Wolf O. T. (2005). Impaired memory retrieval after psychosocial stress in healthy young men. J. Neurosci. 25 2977–2982. 10.1523/jneurosci.5139-04.2005
    1. Lange M., Giffard B., Noal S., Rigal O., Kurtz J. E., Heutte N., et al. (2014). Baseline cognitive functions among elderly patients with localised breast cancer. Eur. J. Cancer 50 2181–2189. 10.1016/j.ejca.2014.05.026
    1. Lehrl S. (1999). Mehrfachwahl-Wortschatz-Intelligenztest MWT-B. Balingen: Spitta-Verlag.
    1. Lehto R. H., Cimprich B. (1999). Anxiety and directed attention in women awaiting breast cancer surgery. Oncol. Nurs. Forum 26 767–772.
    1. Li J., Yu L., Long Z., Li Y., Cao F. (2015). Perceived cognitive impairment in Chinese patients with breast cancer and its relationship with post-traumatic stress disorder symptoms and fatigue. Psychooncology 24 676–682. 10.1002/pon.3710
    1. Li M., Caeyenberghs K. (2018). Longitudinal assessment of chemotherapy-induced changes in brain and cognitive functioning: a systematic review. Neurosci. Biobehav. Rev. 92 304–317. 10.1016/j.neubiorev.2018.05.019
    1. Lindner O. C., Phillips B., McCabe M. G., Mayes A., Wearden A., Varese F., et al. (2014). A meta-analysis of cognitive impairment following adult cancer chemotherapy. Neuropsychology 28 726–740. 10.1037/neu0000064
    1. Mandelblatt J. S., Stern R. A., Luta G., McGuckin M., Clapp J. D., Hurria A., et al. (2014). Cognitive impairment in older patients with breast cancer before systemic therapy: is there an interaction between cancer and comorbidity? J. Clin. Oncol. 32 1909–1918. 10.1200/JCO.2013.54.2050
    1. Menning S., de Ruiter M. B., Veltman D. J., Koppelmans V., Kirschbaum C., Boogerd W., et al. (2015). Multimodal MRI and cognitive function in patients with breast cancer prior to adjuvant treatment–the role of fatigue. Neuroimage Clin. 7 547–554. 10.1016/j.nicl.2015.02.005
    1. Monje M., Dietrich J. (2012). Cognitive side effects of cancer therapy demonstrate a functional role for adult neurogenesis. Behav. Brain Res. 227 376–379. 10.1016/j.bbr.2011.05.012
    1. Patel S. K., Wong A. L., Wong F. L., Breen E. C., Hurria A., Smith M., et al. (2015). Inflammatory biomarkers, comorbidity, and neurocognition in women with newly diagnosed breast cancer. J. Natl. Cancer Inst. 107:djv131. 10.1093/jnci/djv131
    1. Podsakoff P. M., MacKenzie S. B., Lee J. Y., Podsakoff N. P. (2003). Common method biases in behavioral research: a critical review of the literature and recommended remedies. J. Appl. Psychol. 88 879–903. 10.1037/0021-9010.88.5.879
    1. Reid-Arndt S. A., Cox C. R. (2012). Stress, coping and cognitive deficits in women after surgery for breast cancer. J Clin Psychol Med Settings 19 127–137. 10.1007/s10880-011-9274-z
    1. Reitan R. M. (1992). Trail Making Test: Manual for administration and scoring. Tucson, AZ: Neuropsychology Laboratory.
    1. Rick O., Reuss-Borst M., Dauelsberg T., Hass H. G., Konig V., Caspari R., et al. (2018). NeuroCog FX study: a multicenter cohort study on cognitive dysfunction in patients with early breast cancer. Psychooncol 27 2016–2022. 10.1002/pon.4763
    1. Schagen S. B., Muller M. J., Boogerd W., Mellenbergh G. J., van Dam F. S. (2006). Change in cognitive function after chemotherapy: a prospective longitudinal study in breast cancer patients. J. Natl. Cancer Inst. 98 1742–1745. 10.1093/jnci/djj470
    1. Schagen S. B., van Dam F. S., Muller M. J., Boogerd W., Lindeboom J., Bruning P. F. (1999). Cognitive deficits after postoperative adjuvant chemotherapy for breast carcinoma. Cancer 85 640–650. 10.1002/(sici)1097-0142(19990201)85:3<640::aid-cncr14>;2-g
    1. Schellig D., Schächtele B. (2009). Visueller Und Verbaler Merkfähigkeitstest. Göttingen: Hogrefe.
    1. Schilder C. M., Seynaeve C., Linn S. C., Boogerd W., Beex L. V., Gundy C. M., et al. (2012). Self-reported cognitive functioning in postmenopausal breast cancer patients before and during endocrine treatment: findings from the neuropsychological TEAM side-study. Psychooncol 21 479–487. 10.1002/pon.1928
    1. Schrepf A., Lutgendorf S. K., Pyter L. M. (2015). Pre-treatment effects of peripheral tumors on brain and behavior: neuroinflammatory mechanisms in humans and rodents. Brain Behavior Immun 49 1–17. 10.1016/j.bbi.2015.04.010
    1. Schwabe L., Wolf O. T. (2013). Stress and multiple memory systems: from ‘thinking’ to ‘doing’. Trends Cogn Sci 17 60–68. 10.1016/j.tics.2012.12.001
    1. Seigers R., Fardell J. E. (2011). Neurobiological basis of chemotherapy-induced cognitive impairment: a review of rodent research. Neurosci. Biobehav. Rev. 35 729–741. 10.1016/j.neubiorev.2010.09.006
    1. Senf B., Brandt H., Dignass A., Kleinschmidt R., Kaiser J. (2010). Psychosocial distress in acute cancer patients assessed with an expert rating scale. Support Care Cancer 18 957–965. 10.1007/s00520-010-0850-9
    1. Silberfarb P. M. (1983). Chemotherapy and cognitive defects in cancer patients. Ann Rev Med 34 35–46. 10.1146/annurev.me.34.020183.000343
    1. Silverman D. H., Dy C. J., Castellon S. A., Lai J., Pio B. S., Abraham L., et al. (2007). Altered frontocortical, cerebellar, and basal ganglia activity in adjuvant-treated breast cancer survivors 5-10 years after chemotherapy. Breast Cancer Research Treat 103 303–311. 10.1007/s10549-006-9380-z
    1. Simo M., Rifa-Ros X., Rodriguez-Fornells A., Bruna J. (2013). Chemobrain: a systematic review of structural and functional neuroimaging studies. Neurosci. Biobehav. Rev. 37 1311–1321. 10.1016/j.neubiorev.2013.04.015
    1. Snaith R. P., Zigmond A. S. (1986). The hospital anxiety and depression scale. Br Med J (Clin Res Ed) 292:344.
    1. Van Arsdale A., Rosenbaum D., Kaur G., Pinto P., Kuo D. Y., Barrera R., et al. (2016). Prevalence and factors associated with cognitive deficit in women with gynecologic malignancies. Gynecol. Oncol. 141 323–328. 10.1016/j.ygyno.2016.03.001
    1. van Dam F. S., Schagen S. B., Muller M. J., Boogerd W., vd Wall E., Droogleever Fortuyn M. E., et al. (1998). Impairment of cognitive function in women receiving adjuvant treatment for high-risk breast cancer: high-dose versus standard-dose chemotherapy. J. Natl. Cancer Inst. 90 210–218. 10.1093/jnci/90.3.210
    1. Vardy J., Rourke S., Tannock I. F. (2007). Evaluation of cognitive function associated with chemotherapy: a review of published studies and recommendations for future research. J Clin Oncol 25 2455–2463. 10.1200/jco.2006.08.1604
    1. Von Ah D., Harvison K. W., Monahan P. O., Moser L. R., Zhao Q., Carpenter J. S., et al. (2009). Cognitive function in breast cancer survivors compared to healthy age- and education-matched women. Clin. Neuropsychol. 23 661–674. 10.1080/13854040802541439
    1. Wefel J. S., Lenzi R., Theriault R. L., Davis R. N., Meyers C. A. (2004). The cognitive sequelae of standard-dose adjuvant chemotherapy in women with breast carcinoma: results of a prospective, randomized, longitudinal trial. Cancer 100 2292–2299. 10.1002/cncr.20272
    1. Wirkner J., Weymar M., Low A., Hamm C., Struck A. M., Kirschbaum C., et al. (2017). Cognitive functioning and emotion processing in breast cancer survivors and controls: an ERP pilot study. Psychophysiol 54 1209–1222. 10.1111/psyp.12874
    1. Yang Y., Hendrix C. C. (2018). Cancer-related cognitive impairment in breast cancer patients: influences of psychological variables. Asia Pac J Oncol Nurs 5 296–306. 10.4103/apjon.apjon_16_18

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