eISSN: 1897-4309
ISSN: 1428-2526
Contemporary Oncology/Współczesna Onkologia
Current issue Archive Manuscripts accepted About the journal Supplements Addendum Special Issues Abstracting and indexing Subscription Contact Instructions for authors
SCImago Journal & Country Rank
1/2017
 
Share:
Share:
more
 
 
Review paper

A systemic literature review of neuroimaging studies in women with breast cancer treated with adjuvant chemotherapy

Paulina Andryszak, Monika Wiłkość, Paweł Izdebski, Bogdan Żurawski

Contemp Oncol (Pozn) 2017; 21 (1): 6-15
Article file
- A systremic.pdf  [0.09 MB]
 
 

Introduction

The results of neuropsychological examinations carried out over the last two decades indicate the occurrence of cognitive impairments in patients with breast cancer who received chemotherapy [1]. A recent metaanalysis [2] showed a decrease in capacity of attention and selective attention as well as in immediate and delayed verbal recall in patients treated with chemotherapy compared to healthy persons. Changes observed during neuropsychological testing are corroborated by the results of neuroimaging studies carried out in the recent years [3–18].
The aim of this paper is to analyse the results of the neuroimaging studies conducted to date, assessing the cerebral alterations of women with breast cancer treated with chemotherapy.
The paper first focuses on the mechanisms underlying the cognitive decline, then describes the results of the studies on the structural and functional changes in the brain, and finally reports on the compensatory mechanisms observed in chemotherapy-treated women with breast cancer.

Mechanisms of chemotherapy-induced cognitive impairments

The mechanisms of cognitive impairment after chemotherapy (CTx) are still not fully understood [19, 20]. The potential role of various factors is indicated, related both to individual characteristics (host-related, soil characteristics) and the neoplastic disease itself (disease-related, seed characteristics) [21].
Research results imply a direct neurotoxic effect of cytostatic agents, which cross the blood-brain barrier causing, for exzample damage to neurons or glial cells, changes in neurotransmitter levels [22–26], and microvascular damage related to ischemia and brain damage, such as decreased vascular density in the hippocampus after the use of methotrexate [19, 27]. The indirect mechanisms are associated with the deregulation of the immune system and/or release cytokines [22, 28, 29], hormonal changes, e.g., decreased levels of oestrogen and progesterone due to premature menopause [30, 31], or DNA damage due to the effect of oxidative stress and accelerated telomere shortening [22, 28]. Moreover, the significance of individual factors associated with age, vascular risk factors, or the pre-cancer level of cognitive functioning and the amount of cognitive reserves, is also pointed out [31].
The results of more recent studies indicate that some patients may exhibit genetic predisposition to cognitive impairments [20, 31]. A relationship has been shown between the allele 4 of apolipoprotein E (APOE) gene and the deterioration of cognitive functioning in patients previously treated for breast cancer or lymphoma [26]. It was also found that persons with the catechol-O-methyltransferase (COMT)-Val genotype are more susceptible to the negative effects of CTx on cognitive functioning [32]. Genetic polymorphism may be related to the effectiveness of the blood-brain barrier (e.g. different expression of the multidrug resistance gene encoding P-glycoprotein, MDR1), the functioning of cytokines (e.g. polymorphism of the interleukin 6 cytokine gene), neurotransmitters (e.g. the polymorphism of COMT gene), and DNA repair mechanisms (e.g. the polymorphism of the X-ray repair cross complementing protein gene, XRCC1) [22, 33].

Methods

A comprehensive literature search was conducted using the PubMed database. The following search terms and their derivatives were used: cognition, neuroimaging, fMRI, PET, MRI, chemotherapy, breast cancer. Studies had to assess brain functioning with neuroimaging methods, be published in a peer-reviewed journal, and be available as full text in English language. No time period was specified.

Results

Forty-one studies fulfilled the inclusion criteria and were selected for further analysis. Changes in the central nervous system of women with breast cancer (BC) treated with CTx were assessed in 15 studies using an MRI [6, 10–13, 34–43] and in 24 studies using functional neuroimaging methods [3, 5, 7–9, 14–18, 44–57]. In two studies both structural and functional changes were assessed [4, 58]. The characteristics of structural and functional studies in breast cancer patients are presented in Tables 1–4.

Structural changes in the central nervous system of women with breast cancer treated with chemotherapy

In ten studies researchers used Voxel-Based Morphometry (VBM) [4, 6, 12, 37–42, 58] to compare the volume of brain areas and the density of grey and white matter [59]. In five studies Diffusion-Tensor Imaging (DTI) [11, 35, 36, 38, 43] was used to measure the microstructural integrity of white matter using fractional anisotropy (FA) and structural connectivity of the brain [60] was applied. In one study semi-automatic segmentation procedure was used [34] and in three automatic seqmentation procedure were used [10, 13, 39]. Most of the studies were conducted in cross-sectional design: 10 in breast cancer survivors treated with CTx [4, 6, 10, 13, 34, 35, 38–40, 43] and 2 in breast cancer patients prior to CTx [41, 58]; 5 studies were conducted with longitudinal design [11, 36, 37, 61, 62]. The results obtained from breast cancer patients treated with CTx were compared to breast cancer patient without CTx [34, 38, 55], healthy controls [4, 10, 13, 35, 40, 41, 62], non-cancer reference subjects [39, 43], or breast cancer patients without CTx and healthy controls [6, 36, 37, 58, 61]. In four studies breast cancer patients were treated with the same schema of CTx [38, 39, 43, 58] and in the other studies different schemas were applied [4, 6, 10–13, 34–37, 40, 42]. A summary of the structural cerebral changes described in analyzed studies is presented in Table 1.
The evaluation of the anatomical properties of the brain using MRI yields information on the structural changes occurring over time and makes it possible to discern the differences between groups. As already mentioned in the discussion of some of the studies, supplementing the research using MRI with functional imaging techniques is a method to obtain fuller descriptions of chemotherapy-related cognitive impairment (CRCI) [63].

Functional changes in the central nervous system of women with breast cancer treated with chemotherapy

The functional studies were carried out using fMRI [4, 5, 7, 8, 14–16, 18, 48–55, 57, 58, 64], EEG [44, 45, 65], resting state fMRI [3, 17], PET [9] and Pulsed Arterial Spin Labelling MRI Perfusion [56]. During fMRI cognitive processes were assessed using verbal and visual working memory tasks [4, 8, 18, 46, 48, 49, 52–54], visual memory task [5, 57], verbal memory task [9, 14–16], attention [53] and executive functioning [5, 7, 41, 55, 57]. Most studies were conducted in cross-sectional design: 14 in breast cancer survivors treated with CTx [3–5, 7, 9, 14, 16, 17, 44–46, 51, 57, 65] and 4 in breast cancer patient prior to CTx [48–50, 58]; 8 studies were conducted in longitudinal design [8, 15, 18, 52–56]. The results obtained by breast cancer patients treated with CTx were compared with breast cancer patients without CTx [7, 8, 16, 18, 38, 44, 45, 54–56], with breast cancer patients treated with different schemas of CTx [9, 16, 45, 57, 65], with patients treated with radiotherapy [57], with healthy controls [3, 4, 8, 14, 15, 18, 46, 48, 52, 57], or non-cancer reference subjects [49, 50] or with breast cancer patients without CTx and healthy controls [7–9, 18, 51, 54–56]. In three studies breast cancer patients were treated with the same schema of CTx [44, 45, 65], and in the others studies different schemas were applied [3, 4, 7, 8, 14–18, 45–48, 50–57].
Summary of functional changes described in the analysed studies (Table 2).

Compensatory mechanisms

An interesting study to observe the mechanism underlying the process of coping with cognitive demand was performed on 60-year-old homozygous twin sisters [46]. One of the sisters was previously (22 months earlier) treated for breast cancer that AC+T adjuvant chemotherapy (four cycles of AC followed by four cycles of T – docetaxel), and received hormonal therapy (tamoxifen) during the study. While diseases and therapies which could negatively affect cognitive functioning were excluded in both sisters, they were found to have the allele 4 of apolipoprotein E, associated with the occurrence of cognitive deficits [26]. Cognitive functioning was evaluated using standard neuropsychological tests, a self-assessment questionnaire, and functional magnetic resonance imaging (fMRI). It was found that the twin treated with CTx reported much greater problems with cognitive functioning. Nevertheless, the results of the performed neuropsychological tests lay within the norm and differed minimally from those of the healthy sister. The fMRI results showed white matter hyperintensities in both sisters, which are also observed among the carriers of the allele 4 of apolipoprotein E [66, 67]. No coherent pattern of the differences in the volumes of selected brain areas (including the hippocampus, amygdala, frontal part of the hippocampal gyrus cortex, and corpus callosum) were found between sisters. Nonetheless, interesting results were obtained in an fMRI examination during the performance of a task evaluating working memory using the n-back paradigm. It was shown that the more the task was taxing to the working memory, the greater was the scope of activation of brain areas (bilateral stimulation of frontal and parietal areas) in the sister treated with CTx compared to the healthy one. However, no significant differences in the task performance level were observed [64].
The obtained results indicate that in order to enable the adequate performance level of a task by the twin treated with CTx, it was necessary to activate a greater area of neural networks, which most likely requires greater mental effort, reflected in the greater number of complaints about cognitive functioning [64, 68]. It may be supposed that, if the task were made increasingly more taxing, at a certain level of difficulty the compensation for the deficits would be insufficient and the test results would become poorer [68]. The activation of larger areas of the brain in order to maintain the appropriate performance level in cognitive tasks was also confirmed by numerous studies on people aging normally [69–71].
The activation of compensatory mechanisms was also confirmed in a more recent longitudinal study carried out by McDonald, Conroy, Ahles, West, and Saykin [8], which assessed working memory using the n-back paradigm and brain activation using fMRI in women with breast cancer and in healthy ones. The measurements were taken three times: before chemotherapy, and one month, and one year after treatment. The performance level of n-back tasks did not differ significantly between groups; however, changes in activation patterns were observed in all three measurements, both during greater and lesser working memory-loaded tasks. Moreover, greater activation of prefrontal areas was found in the examinations before and one year after the treatment.
Thanks to compensatory neuroplasticity, the cognitive functioning of people treated with chemotherapy can be maintained on an unchanged or only slightly deteriorated level compared to their premorbid abilities. The studies on the levels of brain activation carried out with fMRI revealed that additional brain areas become involved in the performance of lower difficulty tasks, allowing their performance to remain within the norm. A deterioration in functioning becomes visible when the increasing difficulty exceeds the efficiency of compensatory mechanisms [68].

Conclusions

Based on the studies carried out using neuroimaging methods, it is possible to describe the cognitive deficits caused by adjuvant chemotherapy [72]. Specific, albeit small, structural changes and functional changes within the central nervous system are associated with the minor specific impairments of cognitive functions described in literature [72].
The changes in the activity of various cerebral regions in patients treated with chemotherapy indicate that the brain functions in an altered way, by activating new areas or creating new neural connections to reach the same cognitive efficiency. A greater expenditure of energy on mental activities can lead to increased fatigue and be associated with the deterioration in cognitive effectiveness and quality of life suffered by the patients [63]. Even though neuroimaging methods are not free from limitations, using them in CRCI studies in combination with self-descriptive and neuropsychological methods may yield a broader image of the described phenomenon [72].

The authors declare no conflict of interest.

References

1. Wefel JS, Vardy J, Ahles T, Schagen SB. International Cognition and Cancer Task Force recommendations to harmonise studies of cognitive function in patients with cancer. Lancet Oncol 2011; 12: 703-8.
2. Lindner OC, Phillips B, McCabe MG, Mayes A, Wearden A, Varese F, Talmi D. A meta-analysis of cognitive impairment following adult cancer chemotherapy. Neuropsychology 2014; 28: 726-40.
3. Bruno J, Hosseini SM, Kesler S. Altered resting state functional brain network topology in chemotherapy-treated breast cancer survivors. Neurobiol Dis 2012; 48: 329-38.
4. Conroy SK, McDonald BC, Smith DJ, et al. Alterations in brain structure and function in breast cancer survivors: effect of post-chemotherapy interval and relation to oxidative DNA damage. Breast Cancer Res Treat 2013; 137: 493-502.
5. de Ruiter MB, Reneman L, Boogerd W, Veltman DJ, van Dam FS, Nederveen AJ, Boven E, Schagen SB. Cerebral hyporesponsiveness and cognitive impairment 10 years after chemotherapy for breast cancer. Hum Brain Mapp 2011; 32: 1206-9.
6. Inagaki M, Yoshikawa E, Matsuoka Y, et al. Smaller regional volumes of brain gray and white matter demonstrated in breast cancer survivors exposed to adjuvant chemotherapy. Cancer 2007; 109: 146-56.
7. Kesler SR, Kent JS, O’Hara R. Prefrontal cortex and executive function impairments in primary breast cancer. Arch Neurol 2011; 68: 1447-53.
8. McDonald BC, Conroy SK, Ahles TA, West JD, Saykin AJ. Alterations in brain activation during working memory processing associated with breast cancer and treatment: a prospective functional magnetic resonance imaging study. J Clin Oncol 2012; 30: 2500-8.
9. Silverman DH, Dy CJ, Castellon S, et al. Altered frontocortical, cerebellar, and basal ganglia activity in adjuvant-treated breast cancer survivors 5–10 years after chemotherapy. Breast Cancer Res Treat 2007; 103: 303-11.
10. Bergouignan L, Lefranc JP, Chupin M, Morel N, Spano JP, Fossati P. Breast cancer affects both the hippocampus volume and the episodic autobiographical memory retrieval. PLoS One 2011; 6: e25349.
11. Deprez S, Amant F, Smeets A, et al. Longitudinal assessment of chemotherapy-induced structural changes in cerebral white matter and its correlation with impaired cognitive functioning. J Clin Oncol 2012; 30: 274-81.
12. McDonald BC, Conroy SK, Smith DJ, West JD, Saykin AJ. Frontal gray matter reduction after breast cancer chemotherapy and association with executive symptoms: A replication and extension study. Brain Behav Immun 2013; 30 Suppl: S117-25.
13. Kesler SR, Janelsins M, Koovakkattu D, Palesh O, Mustian K, Morrow G, Dhabhar FS. Reduced hippocampal volume and verbal memory performance associated with interleukin-6 and tumor necrosis factor-alpha levels. Brain Behav Immun 2013; 30 Suppl: S109-16.
14. Kesler SR, Bennett FC, Mahaffey ML, Spiegel D. Regional brain activation during verbal declarative memory in metastatic breast cancer. Clin Cancer Res 2009; 15: 6665-73.
15. López Zunini RA, Scherling C, Wallis N, Collins B, MacKenzie J, Bielajew C, Smith AM. Differences in verbal memory retrieval in breast cancer chemotherapy patients compared to healthy controls: a prospective fMRI study. Brain Imaging Behav 2013; 7: 460-77.
16. Kesler SR, Blayney DW. Neurotoxic effects of anthracycline- vs nonanthracycline-based chemotherapy on cognition in breast cancer survivors. JAMA Oncol 2016; 2: 185-92.
17. Piccirillo JF, Hardin FM, Nicklaus J, et al. Cognitive impairment after chemotherapy related to atypical network architecture for executive control. Oncology 2015; 88: 360-8.
18. Jung MS, Zhang M, Askren MK, et al. Cognitive dysfunction and symptom burden in women treated for breast cancer: a prospective behavioral and fMRI analysis. Brain Imaging Behav 2016; doi: 10.1007/s11682-016-9507-8.
19. Staat K, Segatore M. The phenomenon of chemo brain. Clin J Oncol Nursing 2005; 9: 713-21.
20. Vardy J, Tannock I. Cognitive function after chemotherapy in adults with solid tumours. Crit Rev Oncol Hematol 2007; 63: 183-202.
21. Taillibert S. Is systemic anti-cancer therapy neurotoxic? Does chemo brain exist? And should we rename it? Adv Exp Med Biol 2010; 678: 86-95.
22. Ahles TA, Saykin AJ. Candidate mechanisms for chemotherapy-induced cognitive changes. Nat. Rev. Cancer 2007; 7: 192-201.
23. Dietrich J, Han R, Yang Y, Mayer-Pröschel M, Noble M. CNS progenitor cells and oligodendrocytes are targets of chemotherapeutic agents in vitro and in vivo. J Biol 2006; 5: 22.
24. Tuxen MK, Hansen SW. Neurotoxicity secondary to antineoplastic drugs. Cancer Treat Rev 1994; 20: 191-214.
25. Troy L, McFarland K, Littman-Power S, Kelly BJ, Walpole ET, Wyld D, Thomson D. Cisplatin-based therapy: a neurological and neuropsychological review. Psychooncology 2000; 9: 29-39.
26. Ahles TA, Saykin AJ, Noll WW, Furstenberg CT, Guerin S, Cole B, Mott LA. The relationship of APOE genotype to neuropsychological performance in long-term cancer survivors treated with standard dose chemotherapy. Psychooncology 2003; 12: 612-9.
27. Seigers R, Timmermans J, van der Horn HJ et al. Methotrexate reduces hippocampal blood vessel density and activates microglia in rats but does not elevate central cytokine release. Behav Brain Res 2010; 207: 265-72.
28. Barton D, Loprinzi C. Novel approaches to preventing chemotherapy-induced cognitive dysfunction in breast cancer: the art of the possible. Clin Breast Cancer 2002; 3 Suppl 3: S121-7.
29. Fillit HM, Butler RN, O’Connell AW, et al. Achieving and maintaining cognitive vitality with aging. Mayo Clin Proc 2002; 77: 681-96.
30. Ahles TA. Do systemic cancer treatments affect cognitive function? Lancet Oncol 2004; 5: 270-1.
31. Koppelmans V, Breteler MM, Boogerd W, Seynaeve C, Schagen SB.. Late effects of adjuvant chemotherapy for adult onset non-CNS cancer; cognitive impairment, brain structure and risk of dementia. Crit Rev Oncol Hematol 2013; 88: 87-101.
32. Small BJ, Rawson KS, Walsh E, Jim HS, Hughes TF, Iser L, Andrykowski MA, Jacobsen PB. Catechol-O-methyltransferase genotype modulates cancer treatment-related cognitive deficits in breast cancer survivors. Cancer 2011; 117: 1369-76.
33. Vardy J, Wefel JS, Ahles T, Tannock IF, Schagen SB. Cancer and cancer-therapy related cognitive dysfunction: an international perspective from the Venice cognitive workshop. Ann Oncol 2007; 19: 623-9.
34. Yoshikawa E, Matsuoka Y, Inagaki M et al. No adverse effects of adjuvant chemotherapy on hippocampal volume in Japanese breast cancer survivors. Breast Cancer Res Treat 2005; 92: 81-4.
35. Abraham J, Haut MW, Moran MT, Filburn S, Lemiuex S, Kuwabara H. Adjuvant chemotherapy for breast cancer: effects on cerebral white matter seen in diffusion tensor imaging. Clin Breast Cancer 2008; 8: 88-91.
36. Deprez S, Amant F, Yigit R, et al. Chemotherapy-induced structural changes in cerebral white matter and its correlation with impaired cognitive functioning in breast cancer patients. Hum Brain Mapp 2011; 32: 480-93.
37. McDonald BC, Conroy SK, Ahles TA, West JD, Saykin AJ. Gray matter reduction associated with systemic chemotherapy for breast cancer: a prospective MRI study. Breast Cancer Res Treat 2010; 123: 819-28.
38. de Ruiter MB, Reneman L, Boogerd W, et al. Late effects of high-dose adjuvant chemotherapy on white and gray matter in breast cancer survivors: Converging results from multimodal magnetic resonance imaging. Hum. Brain Mapp 2012; 33: 2971-83.
39. Koppelmans V, De Ruiter MB, Van Der Lijn F, et al. Global and focal brain volume in long-term breast cancer survivors exposed to adjuvant chemotherapy. Breast Cancer Res Treat 2012; 132: 1099-106.
40. Hosseini SM, Koovakkattu D, Kesler SR. Altered small-world properties of gray matter networks in breast cancer. BMC Neurol 2012; 12: 28.
41. Scherling C, Collins B, MacKenzie J, Lepage C, Bielajev C, Smith A. Structural brain differences in breast cancer patients compared to matched controls prior to chemotherapy. Int J Biol 2012; 4: 3.
42. Lepage C, Smith AM, Moreau J, Barlow-Krelina E, Wallis N, Collins B, MacKenzie J, Scherling C. A prospective study of grey matter and cognitive function alterations in chemotherapy-treated breast cancer patients. Springerplus 2014; 3: 444.
43. Koppelmans V, Vernooij MW, Boogerd W, Seynaeve C, Ikram MA, Breteler MM, Schagen SB. Prevalence of cerebral small-vessel disease in long-term breast cancer survivors exposed to both adjuvant radiotherapy and chemotherapy. J Clin Oncol 2015; 33: 588-93.
44. Kreukels BP, Schagen SB, Ridderinkhof KR, Boogerd W, Hamburger HL, van Dam FS. Electrophysiological correlates of information processing in breast-cancer patients treated with adjuvant chemotherapy. Breast Cancer Res Treat 2005; 94: 53-61.
45. Kreukels BP, Schagen SB, Ridderinkhof KR, Boogerd W, Hamburger HL, Muller MJ, van Dam FS. Effects of high-dose and conventional-dose adjuvant chemotherapy on long-term cognitive sequelae in patients with breast cancer: an electrophysiologic study. Clin Breast Cancer 2006; 7: 67-78.
46. Ferguson RJ, McDonald BC, Saykin AJ, Ahles TA. Brain structure and function differences in monozygotic twins: possible effects of breast cancer chemotherapy. J Clin Oncol 2007; 25: 3866-70.
47. Kreukels BP, van Dam FS, Ridderinkhof KR, Boogerd W, Schagen SB. Persistent neurocognitive problems after adjuvant chemotherapy for breast cancer. Clin Breast Cancer 2008; 8: 80-7.
48. Cimprich B, Reuter-Lorenz P, Nelson J, et al. Prechemotherapy alterations in brain function in women with breast cancer. J Clin Exp Neuropsychol 2010; 32: 324-31.
49. Scherling C, Collins B, Mackenzie J, et al. Pre-chemotherapy differences in visuospatial working memory in breast cancer patients compared to controls: an FMRI study. Front Hum Neurosci 2011; 5: 122.
50. Scherling C, Collins B, Mackenzie J, Bielajev C, Smith A. Prechemotherapy differences in response inhibition in breast cancer patients compared to controls: a functional magnetic resonance imaging study. J Clin Exp Neuropsychol 2012; 34: 543-60.
51. Kesler SR, Wefel JS, Hosseini SM, Cheung M, Watson CL, Hoeft F. Default mode network connectivity distinguishes chemotherapy-treated breast cancer survivors from controls. Proc Natl Acad Sci U S A 2013; 110: 11600-5.
52. Conroy SK, McDonald BC, Ahles TA, West JD, Saykin AJ. Chemotherapy-induced amenorrhea: a prospective study of brain activation changes and neurocognitive correlates. Brain Imaging Behav 2013; 7: 491-500.
53. Dumas JA, Makarewicz J, Schaubhut GJ, Devins R, Albert K, Dittus K, Newhouse PA. Chemotherapy altered brain functional connectivity in women with breast cancer: a pilot study. Brain Imaging Behav 2013; 7: 524-32.
54. Askren MK, Jung M, Berman MG, et al. Neuromarkers of fatigue and cognitive complaints following chemotherapy for breast cancer: a prospective fMRI investigation. Breast Cancer Res Treat 2014; 147: 445-55.
55. Deprez S, Vandenbulcke M, Peeters R, Emsell L, Smeets A, Christiaens MR, Amant F, Sunaert S. Longitudinal assessment of chemotherapy-induced alterations in brain activation during multitasking and its relation with cognitive complaints. J Clin Oncol 2014; 32: 2031-8.
56. Nudelman KN, Wang Y, McDonald BC, et al. Altered cerebral blood flow one month after systemic chemotherapy for breast cancer: a prospective study using pulsed arterial spin labeling MRI perfusion. PLoS One 2014; 9: e96713.
57. Stouten-Kemperman MM, de Ruiter MB, Boogerd W, Veltman DJ, Reneman L, Schagen SB. Very late treatment-related alterations in brain function of breast cancer survivors. J Int Neuropsychol Soc 2015; 21: 50-61.
58. Menning S, de Ruiter MB, Veltman DJ, Koppelmans V, Kirschbaum C, Boogerd W, Reneman L, Schagen SB. Multimodal MRI and cognitive function in patients with breast cancer prior to adjuvant treatment – the role of fatigue. Neuroimage Clin 2015; 7: 547-54.
59. Ashburner J, Friston KJ. Voxel-based morphometry – the methods. Neuroimage 2000; 11 (6 Pt 1): 805-21.
60. Le Bihan D, Mangin JF, Poupon C, Clark CA, Pappata S, Molko N, Chabriat H. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001; 13: 534-46.
61. McDonald BC, Saykin AJ. Alterations in brain structure related to breast cancer and its treatment: chemotherapy and other considerations. Brain Imaging Behav 2013; 7: 374-87.
62. Lepage M, Habib R, Tulving E. Hippocampal PET activations of memory encoding and retrieval: the HIPER model. Hippocampus 1998; 8: 313-22.
63. Scherling CS, Smith A. Opening up the window into and “chemobrain”: A neuroimaging review. Sensors (Switzerland) 2013; 13: 3169-203.
64. Ferguson CJ. The good, the bad and the ugly: a meta-analytic review of positive and negative effects of violent video games. Psychiatr Q 2007; 78: 309-16.
65. Kreukels BP, Hamburger HL, de Ruiter MB, van Dam FS, Ridderinkhof KR, Boogerd W, Schagen SB. ERP amplitude and latency in breast cancer survivors treated with adjuvant chemotherapy. Clin Neurophysiol 2008; 119: 533-41.
66. Honea RA, Vidoni E, Harsha A, Burns JM. Impact of APOE on the Healthy Aging Brain: A Voxel-Based MRI and DTI Study. J Alzheimers Dis 2008; 18: 553-64.
67. Persson J, Lind J, Larsson A, et al. Altered brain white matter integrity in healthy carriers of the APOE epsilon4 allele: a risk for AD? Neurology 2006; 66: 1029-33.
68. Reuter-Lorenz PA, Cimprich B. Cognitive function and breast cancer: Promise and potential insights from functional brain imaging. Breast Cancer Res Treat 2013; 137: 33-43.
69. Cappell KA, Gmeindl L, Reuter-Lorenz PA. Age differences in prefontal recruitment during verbal working memory maintenance depend on memory load. Cortex 2010; 46: 462-73.
70. Eyler LT, Sherzai A, Kaup AR, Jeste DV. A review of functional brain imaging correlates of successful cognitive aging. Biol Psychiatry 2011; 70: 115-22.
71. Schneider-Garces NJ, Gordon BA, Brumback-Peltz CR, et al. Span, CRUNCH, and beyond: working memory capacity and the aging brain. J Cogn Neurosci 2010; 22: 655-69.
72. Raffa RB. Imaging as a means of studying chemotherapy-related cognitive impairment. Adv Exp Med Biol 2010; 678: 70-6.

Address for correspondence

Paulina Andryszak
Institute of Psychology
Kazimierz Wielki University in Bydgoszcz
Staffa 1
85-867 Bydgoszcz, Poland
e-mail: pandryszak@gmail.com

Submitted: 13.12.2015
Accepted: 30.09.2016
Copyright: © 2017 Termedia Sp. z o. o. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0) License (http://creativecommons.org/licenses/by-nc-sa/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material, provided the original work is properly cited and states its license.
Quick links
© 2017 Termedia Sp. z o.o. All rights reserved.
Developed by Bentus.
PayU - płatności internetowe