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Intra-individual Variability in Women with Breast Cancer

  • Lori J. Bernstein (a1) (a2), Pamela A. Catton (a3) (a4) and Ian F. Tannock (a4) (a5)

Abstract

Studies assessing cognitive functioning in women treated for breast cancer have used primarily standardized neuropsychological tests and examined accuracy and/or reaction time as outcome measures: they have been inconsistent in identifying the cognitive domains affected and the severity of deficits. In other contexts of neural development and disorders, measures of Intra-individual variability (IIV) have proven useful in identifying subtleties in performance deficits that are not captured by measures of central tendency. This article presents proof of concept that assessing IIV may also increase understanding of the cognitive effects of cancer treatment. We analyzed mean accuracy and reaction time, as well as IIV from 65 women with breast cancer and 28 age and education matched controls who performed the Conner's Continuous Performance Test, a “Go-NoGo” task. Although there were no significant differences between groups using measures of central tendency, there was a group × inter-stimulus interval (ISI) interaction for IIV Dispersion (p < .001). Patient Dispersion was more variable at shorter ISI than controls and less variable at long ISI, suggesting greater sensitivity to presentation speed. Interpretation of IIV differences requires further investigation. Our results suggest that future studies would benefit from designs that allow analysis of IIV measures in studies assessing cognition in cancer survivors. (JINS, 2014, 20, 1–11)

Copyright

Corresponding author

Correspondence and reprint requests to: Lori J. Bernstein, Toronto General Hospital, ELLICSR BCS021, 200 Elizabeth Street, Toronto ON M5G 2C4. E-mail: lori.bernstein@uhn.ca

References

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Ahles, T.A., Root, J.C., Ryan, E.L. (2012). Cancer- and cancer treatment-associated cognitive change: An update on the state of the science. Journal of Clinical Oncology, 30, 36753686. doi:10.1200/JCO.2012.43.0116
Ahles, T.A., Saykin, A. (2001). Cognitive effects of standard-dose chemotherapy in patients with cancer. Cancer Investigation, 19, 812820.
Bellgrove, M.A., Hester, R., Garavan, H. (2004). The functional neuroanatomical correlates of response variability: Evidence from a response inhibition task. Neuropsychologia, 42, 19101916. doi: 10.1016/j.neuropsychologia.2004.05.007
Bielak, A.A., Cherbuin, N., Bunce, D., Anstey, K.J. (2013). Intraindividual variability is a fundamental phenomenon of aging: Evidence from an 8-year longitudinal study across young, middle, and older adulthood. Developmental Psychology, 50, 143151. doi:10.1037/a0032650
Bielak, A.A., Hultsch, D.F., Strauss, E., MacDonald, S.W., Hunter, M.A. (2010). Intraindividual variability is related to cognitive change in older adults: Evidence for within-person coupling. Psychology and Aging, 25, 575586. doi:10.1037/a0019503
Burton, C.L., Strauss, E., Hultsch, D.F., Hunter, M.A. (2009). The relationship between everyday problem solving and inconsistency in reaction time in older adults. Neuropsychology, Development, and Cognition. Section B, Aging, Neuropsychology and Cognition, 16, 607632. doi:10.1080/13825580903167283
Buzy, W.M., Medoff, D.R., Schweitzer, J.B. (2009). Intra-individual variability among children with ADHD on a working memory task: An ex-Gaussian approach. Child Neuropsychology, 15, 441459. doi:10.1080/09297040802646991
Castellanos, F.X., Tannock, R. (2002). Neuroscience of attention-deficit/hyperactivity disorder: The search for endophenotypes. Nature Reviews. Neuroscience, 3, 617628. doi:10.1038/nrn896
Castellon, S.A., Ganz, P.A., Bower, J.E., Petersen, L., Abraham, L., Greendale, G.A. (2004). Neurocognitive performance in breast cancer survivors exposed to adjuvant chemotherapy and tamoxifen. Journal of Clinical and Experimental Neuropsychology, 26, 955969.
Cella, D. (1998). Factors influencing quality of life in cancer patients: Anemia and fatigue. Seminars in Oncology, 25, 4346.
Cella, D., Tulsky, D.S., Gray, G., Sarafian, B., Linn, E., Bonomi, A., Harris, J. (1993). The functional assessment of cancer therapy scale: Development and validation of the general measure. Journal of Clinical Oncology, 11, 570579.
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, 7078.
Coates, A., Abraham, S., Kaye, S.B., Sowerbutts, T., Frewin, C., Fox, R.M., Tattersall, M.H. (1983). On the receiving end--patient perception of the side-effects of cancer chemotherapy. European Journal of Cancer and Clinical Oncology, 19, 203208.
Collins, B., Mackenzie, J., Stewart, A., Bielajew, C., Verma, S. (2009). Cognitive effects of chemotherapy in post-menopausal breast cancer patients 1 year after treatment. Psychooncology, 18, 134143. doi:10.1002/pon.1379
Collins, B., Mackenzie, J., Tasca, G.A., Scherling, C., Smith, A. (2013). Cognitive effects of chemotherapy in breast cancer patients: A dose-response study. Psychooncology, 22, 15171527. doi:10.1002/pon.3163
Conners, C.K. (1994). Conners’ Continuous Performance Test (Version 3.0): Toronto, Canada: Multi-Health Systems.
Conners, C.K. (2000). Conners’ Continuous Performance Test-II: Computer program for Windows technical guide and software manual. North Tonawanda, NY: Multi-Health Systems.
de Ruiter, M.B., Reneman, L., Boogerd, W., Veltman, D.J., Caan, M., Douaud, G., Schagen, S.B. (2012). Late effects of high-dose adjuvant chemotherapy on white and gray matter in breast cancer survivors: Converging results from multimodal magnetic resonance imaging. Human Brain Mapping, 33, 29712983. doi:10.1002/hbm.21422
de Ruiter, M.B., Reneman, L., Boogerd, W., Veltman, D.J., van Dam, F.S., Nederveen, A.J., Schagen, S.B. (2011). Cerebral hyporesponsiveness and cognitive impairment 10 years after chemotherapy for breast cancer. Human Brain Mapping, 32, 12061219. doi:10.1002/hbm.21102
Deprez, S., Amant, F., Smeets, A., Peeters, R., Leemans, A., Van Hecke, W., Sunaert, S. (2012). Longitudinal assessment of chemotherapy-induced structural changes in cerebral white matter and its correlation with impaired cognitive functioning. Journal of Clinical Oncology, 30, 274281. doi:10.1200/JCO.2011.36.8571
Deprez, S., Amant, F., Yigit, R., Porke, K., Verhoeven, J., Van den Stock, J., Sunaert, S. (2011). Chemotherapy-induced structural changes in cerebral white matter and its correlation with impaired cognitive functioning in breast cancer patients. Human Brain Mapping, 32, 480493. doi:10.1002/hbm.21033
Donovan, K.A., Small, B.J., Andrykowski, M.A., Schmitt, F.A., Munster, P., Jacobsen, P.B. (2005). Cognitive functioning after adjuvant chemotherapy and/or radiotherapy for early-stage breast carcinoma. Cancer, 104, 24992507.
Downie, F.P., Mar Fan, H.G., Houede-Tchen, N., Yi, Q., Tannock, I.F. (2006). Cognitive function, fatigue, and menopausal symptoms in breast cancer patients receiving adjuvant chemotherapy: Evaluation with patient interview after formal assessment. Psychooncology, 15, 921930.
Duchek, J.M., Balota, D.A., Tse, C.S., Holtzman, D.M., Fagan, A.M., Goate, A.M. (2009). The utility of intraindividual variability in selective attention tasks as an early marker for Alzheimer's disease. Neuropsychology, 23, 746758. doi:10.1037/a0016583
Dykiert, D., Der, G., Starr, J.M., Deary, I.J. (2012). Age differences in intra-individual variability in simple and choice reaction time: Systematic review and meta-analysis. [Meta-Analysis Research Support, Non-U.S. Gov't Review]. PloS One, 7, e45759. doi:10.1371/journal.pone.0045759
Fallowfield, L.J., Leaity, S.K., Howell, A., Benson, S., Cella, D. (1999). Assessment of quality of life in women undergoing hormonal therapy for breast cancer: Validation of an endocrine symptom subscale for the FACT-B. Breast Cancer Research and Treatment, 55, 189199.
Faust, M.E., Balota, D.A., Spieler, D.H., Ferraro, F.R. (1999). Individual differences in information-processing rate and amount: Implications for group differences in response latency. Psychological Bulletin, 125, 777799.
Ferguson, R.J., McDonald, B.C., Saykin, A.J., Ahles, T.A. (2007). Brain structure and function differences in monozygotic twins: Possible effects of breast cancer chemotherapy. Journal of Clinical Oncology, 25, 38663870.
Flehmig, H.C., Steinborn, M., Langner, R., Scholz, A., Westhoff, K. (2007). Assessing intraindividual variability in sustained attention: Reliability, relation to speed and accuracy, and practice effects. Psychological Science, 49, 132149.
Fogel, B.S. (1991). The high sensitivity cognitive screen. International Psychogeriatrics, 3, 273288.
Folstein, M.F., Folstein, S.E., McHugh, P.R. (1975). “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189198.
Hultsch, D.F., MacDonald, S.W., Dixon, R.A. (2002). Variability in reaction time performance of younger and older adults. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 57, P101P115.
Jackson, J.D., Balota, D.A., Duchek, J.M., Head, D. (2012). White matter integrity and reaction time intraindividual variability in healthy aging and early-stage Alzheimer disease. [Research Support, N.I.H., Extramural]. Neuropsychologia, 50, 357366. doi:10.1016/j.neuropsychologia.2011.11.024
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. Supportive Care in Cancer, 19, 16471656. doi:10.1007/s00520-010-0997-4
Jenkins, V., Shilling, V., Deutsch, G., Bloomfield, D., Morris, R., Allan, S., Winstanley, J. (2006). A 3-year prospective study of the effects of adjuvant treatments on cognition in women with early stage breast cancer. British Journal of Cancer, 94, 828834.
Jim, H.S., Phillips, K.M., Chait, S., Faul, L.A., Popa, M.A., Lee, Y.H., Small, B.J. (2012). Meta-analysis of cognitive functioning in breast cancer survivors previously treated with standard-dose chemotherapy. Journal of Clinical Oncology, 30, 35783587. doi:10.1200/JCO.2011.39.5640
Kesler, S.R., Sheau, K., Koovakkattu, D., Reiss, A.L. (2011). Changes in frontal-parietal activation and math skills performance following adaptive number sense training: Preliminary results from a pilot study. Neuropsychological Rehabilitation, 21, 433454. doi:10.1080/09602011.2011.578446
Kinsinger, S.W., Lattie, E., Mohr, D.C. (2010). Relationship between depression, fatigue, subjective cognitive impairment, and objective neuropsychological functioning in patients with multiple sclerosis. Neuropsychology, 24, 573580. doi:10.1037/a00192222010-17509-003 [pii]
Klein, C., Wendling, K., Huettner, P., Ruder, H., Peper, M. (2006). Intra-subject variability in attention-deficit hyperactivity disorder. Biological Psychiatry, 60, 10881097. doi:10.1016/j.biopsych.2006.04.003
Koppelmans, V., Breteler, M.M., Boogerd, W., Seynaeve, C., Gundy, C., Schagen, S.B. (2012). Neuropsychological performance in survivors of breast cancer more than 20 years after adjuvant chemotherapy. Journal of Clinical Oncology, 30, 10801086. doi:10.1200/JCO.2011.37.0189
Koppelmans, V., Groot, M.D., de Ruiter, M.B., Boogerd, W., Seynaeve, C., Vernooij, M.W., Breteler, M.M. (2012). Global and focal white matter integrity in breast cancer survivors 20 years after adjuvant chemotherapy. Human Brain Mapping doi:10.1002/hbm.22221
Li, S., Aggen, S.H., Nesselroade, J.R., Baltes, P.B. (2001). Short-term fluctuations in elderly people's sensorimotor functioning predict text and spatial memory performance: The Macarthur Successful Aging Studies. Gerontology, 47, 100116. doi:52782
Lovden, M., Li, S.C., Shing, Y.L., Lindenberger, U. (2007). Within-person trial-to-trial variability precedes and predicts cognitive decline in old and very old age: Longitudinal data from the Berlin Aging Study. Neuropsychologia, 45, 28272838. doi:10.1016/j.neuropsychologia.2007.05.005
MacDonald, S.W., Hultsch, D.F., Dixon, R.A. (2003). Performance variability is related to change in cognition: Evidence from the Victoria Longitudinal Study. Psychology and Aging, 18, 510523. doi:10.1037/0882-7974.18.3.510
Maor, Y., Olmer, L., Mozes, B. (2001). The relation between objective and subjective impairment in cognitive function among multiple sclerosis patients--the role of depression. Multiple Sclerosis Journal, 7, 131135.
McDonald, B.C., Conroy, S.K., Ahles, T.A., West, J.D., Saykin, A.J. (2012). Alterations in brain activation during working memory processing associated with breast cancer and treatment: A prospective functional magnetic resonance imaging study. Journal of Clinical Oncology, 30, 25002508. doi:10.1200/JCO.2011.38.5674
Moore, L.H., van Gorp, W.G., Hinkin, C.H., Stern, M.J., Swales, T., Satz, P. (1997). Subjective complaints versus actual cognitive deficits in predominantly symptomatic HIV-1 seropositive individuals. Journal of Neuropsychiatry and Clinical Neurosciences, 9, 3744.
Morgan, E.E., Woods, S.P., Delano-Wood, L., Bondi, M.W., Grant, I. (2011). Intraindividual variability in HIV infection: Evidence for greater neurocognitive dispersion in older HIV seropositive adults. Neuropsychology, 25, 645654. doi:10.1037/a0023792
Myerson, J., Robertson, S., Hale, S. (2007). Aging and intraindividual variability in performance: Analyses of response time distributions. Journal of the Experimental Analysis of Behavior, 88, 319337.
Nesselroade, J.R., Salthouse, T.A. (2004). Methodological and theoretical implications of intraindividual variability in perceptual-motor performance. The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 59, P49P55.
Rabbitt, P., Osman, P., Moore, B., Stollery, B. (2001). There are stable individual differences in performance variability, both from moment to moment and from day to day. The Quarterly Journal of Experimental Psychology. A, Human Experimental Psychology, 54, 9811003. doi:10.1080/713756013
Raffa, R.B., Martin, K.J. (2010). Chemo fog: Cancer chemotherapy-related cognitive impairment. In R. B. Raffa & R. J. Tallarida (Eds.), Advances in experimental medicine and biology: Chemo fog: cancer chemotherapy-related cognitive impairment (Vol. 678, pp. 1112). New York: Landes Bioscience and Springer Science+Business Media, LLC.
Reitan, R.M., Wolfson, D. (1985). The Halstead-Reitan Neuropsychological Test Battery. Tuscon, AZ: Neuropsychology Press.
Robertson, S., Myerson, J., Hale, S. (2006). Are there age differences in intraindividual variability in working memory performance? The Journals of Gerontology. Series B, Psychological Sciences and Social Sciences, 61, 1824.
Samain, E., Schauvliege, F., Deval, B., Marty, J. (2003). Anesthesia for breast cancer surgery in the elderly. Critical Reviews in Oncology/Hematology, 46, 115120.
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. Journal of the National Cancer Institute, 98, 17421745.
Schagen, S.B., Muller, M.J., Boogerd, W., Rosenbrand, R.M., van Rhijn, D., Rodenhuis, S., van Dam, F.S. (2002). Late effects of adjuvant chemotherapy on cognitive function: A follow-up study in breast cancer patients. Annals of Oncology, 13, 13871397.
Scherling, C., Collins, B., Mackenzie, J., Bielajew, C., Smith, A. (2012). Prechemotherapy differences in response inhibition in breast cancer patients compared to controls: A functional magnetic resonance imaging study. Journal of Clinical and Experimental Neuropsychology, 34, 543560. doi:10.1080/13803395.2012.666227
Seruga, B., Zhang, H., Bernstein, L.J., Tannock, I.F. (2008). Cytokines and their relationship to the symptoms and outcome of cancer. Nature Reviews Cancer, 8, 887899. doi:10.1038/nrc2507 nrc2507 [pii]
Shaffer, V.A., Merkle, E.C., Fagerlin, A., Griggs, J.J., Langa, K.M., Iwashyna, T.J. (2012). Chemotherapy was not associated with cognitive decline in older adults with breast and colorectal cancer: Findings from a prospective cohort study. Medical Care, 50, 849855. doi:10.1097/MLR.0b013e31825a8bb0
Shilling, V., Jenkins, V. (2006). Self-reported cognitive problems in women receiving adjuvant therapy for breast cancer. European Journal of Oncology Nursing, 11, 615.
Shilling, V., Jenkins, V., Morris, R., Deutsch, G., Bloomfield, D. (2005). The effects of adjuvant chemotherapy on cognition in women with breast cancer--preliminary results of an observational longitudinal study. Breast, 14, 142150.
Small, B.J., Rawson, K.S., Walsh, E., Jim, H.S., Hughes, T.F., Iser, L., Jacobsen, P.B. (2011). Catechol-O-methyltransferase genotype modulates cancer treatment-related cognitive deficits in breast cancer survivors. Cancer, 117, 13691376. doi:10.1002/cncr.25685
Strauss, E., MacDonald, S.W., Hunter, M., Moll, A., Hultsch, D.F. (2002). Intraindividual variability in cognitive performance in three groups of older adults: Cross-domain links to physical status and self-perceived affect and beliefs. Journal of the International Neuropsychological Society, 8, 893906.
Stuss, D.T., Murphy, K.J., Binns, M.A., Alexander, M.P. (2003). Staying on the job: The frontal lobes control individual performance variability. Brain, 126, 23632380.
Stuss, D.T., Pogue, J., Buckle, L., Bondar, J. (1994). Characterization of statibility of performance in patients with traumatic brain injury: Variability and consistency on reaction time tests. Neuropsychology, 8, 316324.
Stuss, D.T., Stethem, L.L., Hugenholtz, H., Picton, T., Pivik, J., Richard, M.T. (1989). Reaction time after head injury: Fatigue, divided and focused attention, and consistency of performance. Journal of Neurology, Neurosurgery, and Psychiatry, 52, 742748.
Tales, A., Leonards, U., Bompas, A., Snowden, R.J., Philips, M., Porter, G., Bayer, A. (2012). Intra-individual reaction time variability in amnestic mild cognitive impairment: A precursor to dementia? Journal of Alzheimer's Disease, 32, 457466. doi:10.3233/JAD-2012-120505
Tannock, I.F., Ahles, T.A., Ganz, P.A., Van Dam, F.S. (2004). Cognitive impairment associated with chemotherapy for cancer: Report of a workshop. Journal of Clinical Oncology, 22, 22332239.
Tchen, N., Juffs, H.G., Downie, F.P., Yi, Q.L., Hu, H., Chemerynsky, I., Tannock, I.F. (2003). Cognitive function, fatigue, and menopausal symptoms in women receiving adjuvant chemotherapy for breast cancer. Journal of Clinical Oncology, 21, 41754183.
van Dam, F.S., Schagen, S.B., Muller, M.J., Boogerd, W., vd Wall, E., Droogleever Fortuyn, M.E., Rodenhuis, S. (1998). Impairment of cognitive function in women receiving adjuvant treatment for high-risk breast cancer: High-dose versus standard-dose chemotherapy. Journal of the National Cancer Institute, 90, 210218.
van Gorp, W.G., Satz, P., Hinkin, C., Selnes, O., Miller, E.N., McArthur, J., Paz, D. (1991). Metacognition in HIV-1 seropositive asymptomatic individuals: Self-ratings versus objective neuropsychological performance. Multicenter AIDS Cohort Study (MACS). Journal of Clinical and Experimental Neuropsychology, 13, 812819. doi:10.1080/01688639108401091
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. Journal of Clinical Oncology, 25, 24552463.
Vardy, J., Wefel, J.S., Ahles, T., Tannock, I.F., Schagen, S.B. (2008). Cancer and cancer-therapy related cognitive dysfunction: An international perspective from the Venice cognitive workshop. Annals of Oncology, 19, 623629.
Vaurio, R.G., Simmonds, D.J., Mostofsky, S.H. (2009). Increased intra-individual reaction time variability in attention-deficit/hyperactivity disorder across response inhibition tasks with different cognitive demands. Neuropsychologia, 47, 23892396. doi:10.1016/j.neuropsychologia.2009.01.022
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, 22922299.
Wefel, J.S., Saleeba, A.K., Buzdar, A.U., Meyers, C.A. (2010). Acute and late onset cognitive dysfunction associated with chemotherapy in women with breast cancer. Cancer, 116, 33483356. doi:10.1002/cncr.25098
West, R., Murphy, K.J., Armilio, M.L., Craik, F.I., Stuss, D.T. (2002). Lapses of intention and performance variability reveal age-related increases in fluctuations of executive control. Brain and Cognition, 49, 402419.
Wilkins, J.W., Robertson, K.R., Snyder, C.R., Robertson, W.K., van der Horst, C., Hall, C.D. (1991). Implications of self-reported cognitive and motor dysfunction in HIV-positive patients. The American Journal of Psychiatry, 148, 641643.
Yellen, S.B., Cella, D.F., Webster, K., Blendowski, C., Kaplan, E. (1997). Measuring fatigue and other anemia-related symptoms with the Functional Assessment of Cancer Therapy (FACT) measurement system. Journal of Pain and Symptom Management, 13, 6374.
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