Advertisement

Brain Imaging and Behavior

, Volume 7, Issue 4, pp 363–373 | Cite as

Neuroimaging biomarkers and cognitive function in non-CNS cancer and its treatment: Current status and recommendations for future research

  • Andrew J. SaykinEmail author
  • Michiel B. de Ruiter
  • Brenna C. McDonald
  • Sabine Deprez
  • Daniel H. S. Silverman
SI: Neuroimaging Studies of Cancer and Cancer Treatment

Abstract

Cognitive changes in patients undergoing treatment for non-central nervous system (CNS) cancers have been recognized for several decades, yet the underlying mechanisms are not well understood. Structural, functional and molecular neuroimaging has the potential to help clarify the neural bases of these cognitive abnormalities. Structural magnetic resonance imaging (MRI), functional MRI (fMRI), diffusion tensor imaging (DTI), MR spectroscopy (MRS), and positron emission tomography (PET) have all been employed in the study of cognitive effects of cancer treatment, with most studies focusing on breast cancer and changes thought to be induced by chemotherapy. Articles in this special issue of Brain Imaging and Behavior are devoted to neuroimaging studies of cognitive changes in patients with non-CNS cancer and include comprehensive critical reviews and novel research findings. The broad conclusions that can be drawn from past studies and the present body of new research is that there are structural and functional changes associated with cancer and various treatments, particularly systemic cytotoxic chemotherapy, although some cognitive and fMRI studies have identified changes at pre-treatment baseline. Recommendations to accelerate progress include well-powered multicenter neuroimaging studies, a better standardized definition of the cognitive phenotype and extension to other cancers. A systems biology framework incorporating multimodality neuroimaging, genetics and other biomarkers will be highly informative regarding individual differences in risk and protective factors and disease- and treatment-related mechanisms. Studies of interventions targeting cognitive changes are also needed. These next steps are expected to identify novel protective strategies and facilitate a more personalized medicine for cancer patients.

Keywords

Neuroimaging MRI PET Cognition Cancer Chemotherapy Genetics Biomarkers Personalized medicine 

Notes

Acknowledgments

The authors wish to thank the Organizing Committee of the International Cognition and Cancer Task Force (ICCTF; http://www.icctf.com/). This project and special issue are an outgrowth of the Neuroimaging Working Group of the ICCTF. The authors gratefully acknowledge support from the following funding sources. Drs. Saykin and McDonald: Supported in part by the National Cancer Institute (R01 CA101318, P30 CA082709 and R25 CA117865), the National Institute on Aging (R01 AG19771, P30 AG10133), and the National Library of Medicine (R01 LM011360). Dr. de Ruiter: Supported by the Dutch Cancer Society, Grant numbers KWF 2009–4284; KWF 2010–4894; KWF 2012–5495. Dr. Deprez: The Fonds Wetenschappelijk Onderzoek–Vlaanderen (Grant No. G.048010N) and by the Stichting tegen Kanker. Dr. Silverman: National Institute of Neurological Diseases and Stroke (R21 NS071385).

References

  1. Ahles, T. A., & Saykin, A. J. (2007). Candidate mechanisms for chemotherapy-induced cognitive changes. Nature Reviews Cancer, 7(3), 192–201. doi: 10.1038/nrc2073.PubMedCentralPubMedCrossRefGoogle Scholar
  2. Ahles, T. A., Saykin, A. J., Noll, W. W., Furstenberg, C. T., Guerin, S., Cole, B., et al. (2003). The relationship of APOE genotype to neuropsychological performance in long-term cancer survivors treated with standard dose chemotherapy. Psychooncology, 12(6), 612–619. doi: 10.1002/pon.742.PubMedCrossRefGoogle Scholar
  3. 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 Research and Treatment, 110(1), 143–152. doi: 10.1007/s10549-007-9686-5.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 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(30), 3675–3686. doi: 10.1200/JCO.2012.43.0116.PubMedCrossRefGoogle Scholar
  5. American Psychiatric Association. (2013). Diagnostic and Statistical Manual of Mental Disorders (DSM-5).Google Scholar
  6. Anderson-Hanley, C., Sherman, M. L., Riggs, R., Agocha, V. B., & Compas, B. E. (2003). Neuropsychological effects of treatments for adults with cancer: a meta-analysis and review of the literature. Journal of International Neuropsychological Society, 9(7), 967–982. doi: 10.1017/S1355617703970019.Google Scholar
  7. Arndt, J., Das, E., Schagen, S. B., Reid-Arndt, S. A., Cameron, L. D., & Ahles, T. A. (2013). Broadening the cancer and cognition landscape: the role of self-regulatory challenges. Psychooncology. doi: 10.1002/pon.3351.Google Scholar
  8. Bruno, J., Hosseini, S. M., & Kesler, S. (2012). Altered resting state functional brain network topology in chemotherapy-treated breast cancer survivors. Neurobiology of Disease, 48(3), 329–338. doi: 10.1016/j.nbd.2012.07.009.PubMedCentralPubMedCrossRefGoogle Scholar
  9. Cimprich, B., Reuter-Lorenz, P., Nelson, J., Clark, P. M., Therrien, B., Normolle, D., et al. (2010). Prechemotherapy alterations in brain function in women with breast cancer. Journal of Clinical and Experimental Neuropsychology, 32(3), 324–331. doi: 10.1080/13803390903032537.PubMedCrossRefGoogle Scholar
  10. Conroy, S. K., McDonald, B. C., O’Neill, D. P., & Saykin, A. J. (2012). Neuroimaging in cancer and oncology. In C. A. Noggle & R. S. Dean (Eds.), The Neuropsychology of Cancer and Oncology (pp. 235–260): Springer.Google Scholar
  11. Conroy, S. K., McDonald, B. C., Ahles, T. A., West, J. D., & Saykin, A. J. (2013a). Chemotherapy-induced amenorrhea: a prospective study of brain activation changes and neurocognitive correlates. Brain Imaging Behav. doi: 10.1007/s11682-013-9240-5
  12. Conroy, S. K., McDonald, B. C., Smith, D. J., Moser, L. R., West, J. D., Kamendulis, L. M., et al. (2013b). Alterations in brain structure and function in breast cancer survivors: effect of post-chemotherapy interval and relation to oxidative DNA damage. Breast Cancer Research and Treatment, 137(2), 493–502. doi: 10.1007/s10549-012-2385-x.PubMedCrossRefGoogle Scholar
  13. Correa, D. D., Root, J. C., Baser, R., Moore, D., Peck, K. K., Lis, E. et al. (2013). A prospective evaluation of changes in brain structure and cognitive functions in adult stem cell transplant recipients. Brain Imaging Behav. doi: 10.1007/s11682-013-9221-8
  14. de Ruiter, M. B., & Schagen, S. B. (2013). Functional MRI studies in non-CNS cancers. Brain Imaging Behav, 1–21. doi: 10.1007/s11682-013-9249-9
  15. de Ruiter, M. B., Reneman, L., Boogerd, W., Veltman, D. J., van Dam, F. S., Nederveen, A. J., et al. (2011). Cerebral hyporesponsiveness and cognitive impairment 10 years after chemotherapy for breast cancer. Human Brain Mapping, 32(8), 1206–1219. doi: 10.1002/hbm.21102.PubMedCrossRefGoogle Scholar
  16. de Ruiter, M. B., Reneman, L., Boogerd, W., Veltman, D. J., Caan, M., Douaud, G., et al. (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(12), 2971–2983. doi: 10.1002/hbm.21422.PubMedCrossRefGoogle Scholar
  17. 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. Human Brain Mapping, 32(3), 480–493. doi: 10.1002/hbm.21033.PubMedCrossRefGoogle Scholar
  18. 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 and Behavior. doi: 10.1007/s11682-012-9220-1.Google Scholar
  19. Dumas, J. A., Makarewicz, J., Schaubhut, G. J., Devins, R., Albert, K., Dittus, K., et al. (2013). Chemotherapy altered brain functional connectivity in women with breast cancer: a pilot study. Brain Imaging and Behavior. doi: 10.1007/s11682-013-9244-1.PubMedGoogle Scholar
  20. Ercoli, L. M., Castellon, S. A., Hunter, A. M., Kwan, L., Kahn-Mills, B. A., Cernin, P. A. et al. (2013). Assessment of the feasibility of a rehabilitation intervention program for breast cancer survivors with cognitive complaints. Brain Imaging Behav, 1–11. doi: 10.1007/s11682-013-9237-0
  21. Falleti, M. G., Sanfilippo, A., Maruff, P., Weih, L., & Phillips, K. A. (2005). The nature and severity of cognitive impairment associated with adjuvant chemotherapy in women with breast cancer: a meta-analysis of the current literature. Brain and Cognition, 59(1), 60–70. doi: 10.1016/j.bandc.2005.05.001.PubMedCrossRefGoogle Scholar
  22. 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(25), 3866–3870. doi: 10.1200/JCO.2007.10.8639.PubMedCentralPubMedCrossRefGoogle Scholar
  23. Ganz, P. A., Bower, J. E., Kwan, L., Castellon, S. A., Silverman, D. H., Geist, C., et al. (2013). Does tumor necrosis factor-alpha (TNF-alpha) play a role in post-chemotherapy cerebral dysfunction? Brain Behav Immun. Suppl, 30, S99–S108. doi: 10.1016/j.bbi.2012.07.015.Google Scholar
  24. Hodgson, K. D., Hutchinson, A. D., Wilson, C. J., & Nettelbeck, T. (2013). A meta-analysis of the effects of chemotherapy on cognition in patients with cancer. Cancer Treatment Reviews, 39(3), 297–304. doi: 10.1016/j.ctrv.2012.11.001.PubMedCrossRefGoogle Scholar
  25. Holohan, K. N., Lahiri, D. K., Schneider, B. P., Foroud, T., & Saykin, A. J. (2012). Functional microRNAs in Alzheimer's disease and cancer: differential regulation of common mechanisms and pathway. Frontiers in Genetics, 3, 323. doi: 10.3389/fgene.2012.00323.PubMedCentralPubMedGoogle Scholar
  26. Holohan, K. N., Von Ah, D., McDonald, B. C., & Saykin, A. J. (2013a). Neuroimaging, cancer, and cognition: state of the knowledge. Seminars in Oncology Nursing, 29(4), 280–287. doi: 10.1016/j.soncn.2013.08.008.PubMedCrossRefGoogle Scholar
  27. Holohan, K., Wang, Y., McDonald, B., Conroy, S., Smith, D., West, J., et al. (2013b). Cerebral perfusion and cognition after breast cancer chemotherapy: A prospective PASL MRI study. Poster presented at the Annual Meeting of the Organization for Human Brain Mapping, June 16–20, 2013, Seattle, WA.Google Scholar
  28. Hosseini, S. M., Koovakkattu, D., & Kesler, S. R. (2012). Altered small-world properties of gray matter networks in breast cancer. BMC Neurology, 12, 28. doi: 10.1186/1471-2377-12-28.PubMedCentralPubMedCrossRefGoogle Scholar
  29. Inagaki, M., Yoshikawa, E., Matsuoka, Y., Sugawara, Y., Nakano, T., Akechi, T., et al. (2007). Smaller regional volumes of brain gray and white matter demonstrated in breast cancer survivors exposed to adjuvant chemotherapy. Cancer, 109(1), 146–156. doi: 10.1002/cncr.22368.PubMedCrossRefGoogle Scholar
  30. Jansen, C. E., Miaskowski, C. A., Dodd, M. J., & Dowling, G. A. (2007). A meta-analysis of the sensitivity of various neuropsychological tests used to detect chemotherapy-induced cognitive impairment in patients with breast cancer. Oncology Nursing Forum, 34(5), 997–1005. doi: 10.1188/07.ONF.997-1005.PubMedCrossRefGoogle Scholar
  31. Jim, H. S., Phillips, K. M., Chait, S., Faul, L. A., Popa, M. A., Lee, Y. H., et al. (2012). Meta-analysis of cognitive functioning in breast cancer survivors previously treated with standard-dose chemotherapy. Journal of Clinical Oncology, 30(29), 3578–3587. doi: 10.1200/JCO.2011.39.5640.PubMedCrossRefGoogle Scholar
  32. Kesler, S. R., Bennett, F. C., Mahaffey, M. L., & Spiegel, D. (2009). Regional brain activation during verbal declarative memory in metastatic breast cancer. Clinical Cancer Research, 15(21), 6665–6673. doi: 10.1158/1078-0432.CCR-09-1227.PubMedCentralPubMedCrossRefGoogle Scholar
  33. Kesler, S. R., Kent, J. S., & O'Hara, R. (2011). Prefrontal cortex and executive function impairments in primary breast cancer. Archives of Neurology, 68(11), 1447–1453. doi: 10.1001/archneurol.2011.245.PubMedCentralPubMedCrossRefGoogle Scholar
  34. Kesler, S. R., Janelsins, M., Koovakkattu, D., Palesh, O., Mustian, K., Morrow, G., et al. (2013a). Reduced hippocampal volume and verbal memory performance associated with interleukin-6 and tumor necrosis factor-alpha levels in chemotherapy-treated breast cancer survivors. Brain, Behavior, and Immunity, 30(Suppl), S109–S116. doi: 10.1016/j.bbi.2012.05.017.PubMedCentralPubMedCrossRefGoogle Scholar
  35. Kesler, S. R., Watson, C., Koovakkattu, D., Lee, C., O'Hara, R., Mahaffey, M. L., et al. (2013b). Elevated prefrontal myo-inositol and choline following breast cancer chemotherapy. Brain Imaging and Behavior. doi: 10.1007/s11682-013-9228-1.PubMedGoogle Scholar
  36. Kim, L. S., Hwang, H. S., Jon, D. I., Ham, B. J., & Seok, J. H. (2008). Dysfunction of the neural network associated with sustained attention in cancer patients with clinically significant depressive symptoms. Neuroscience Letters, 447(1), 1–6. doi: 10.1016/j.neulet.2008.09.077.PubMedCrossRefGoogle Scholar
  37. Koppelmans, V., de Ruiter, M. B., van der Lijn, F., Boogerd, W., Seynaeve, C., van der Lugt, A., et al. (2012a). Global and focal brain volume in long-term breast cancer survivors exposed to adjuvant chemotherapy. Breast Cancer Research and Treatment, 132(3), 1099–1106. doi: 10.1007/s10549-011-1888-1.PubMedCrossRefGoogle Scholar
  38. Koppelmans, V., Groot, M. D., de Ruiter, M. B., Boogerd, W., Seynaeve, C., Vernooij, M. W., et al. (2012b). Global and focal white matter integrity in breast cancer survivors 20 years after adjuvant chemotherapy. Human Brain Mapping. doi: 10.1002/hbm.22221.PubMedGoogle Scholar
  39. Kroenke, C. H., Kubzansky, L. D., Schernhammer, E. S., Holmes, M. D., & Kawachi, I. (2006). Social networks, social support, and survival after breast cancer diagnosis. Journal of Clinical Oncology, 24(7), 1105–1111. doi: 10.1200/jco.2005.04.2846.PubMedCrossRefGoogle Scholar
  40. Lopez Zunini, R. A., Scherling, C., Wallis, N., Collins, B., Mackenzie, J., Bielajew, C., et al. (2012). Differences in verbal memory retrieval in breast cancer chemotherapy patients compared to healthy controls: a prospective fMRI study. Brain Imaging and Behavior. doi: 10.1007/s11682-012-9213-0.PubMedGoogle Scholar
  41. Mandelblatt, J. S., Hurria, A., McDonald, B. C., Saykin, A. J., Stern, R. A., VanMeter, J. W., . . . For the TLC Study (Thinking and Living with Cancer). (2013, in press). Cognitive effects of cancer and its treatments at the intersection of aging: What do we know; What do we need to know? Seminars in Oncology.Google Scholar
  42. McAllister, T. W., Ahles, T. A., Saykin, A. J., Ferguson, R. J., McDonald, B. C., Lewis, L. D., et al. (2004). Cognitive effects of cytotoxic cancer chemotherapy: predisposing risk factors and potential treatments. Current Psychiatry Reports, 6(5), 364–371.PubMedCrossRefGoogle Scholar
  43. McDonald, B. C., & Saykin, A. J. (2011). Neurocognitive dimensions of breast cancer and its treatment. Neuropsychopharmacology, 36(1), 355–356. doi: 10.1038/npp.2010.142.PubMedCrossRefGoogle Scholar
  44. McDonald, B. C., & Saykin, A. J. (2013). Alterations in brain structure related to breast cancer and its treatment: chemotherapy and other considerations. Brain Imaging Behav, 1–14. doi: 10.1007/s11682-013-9256-x
  45. McDonald, B. C., Conroy, S. K., Ahles, T. A., West, J. D., & Saykin, A. J. (2010). Gray matter reduction associated with systemic chemotherapy for breast cancer: a prospective MRI study. Breast Cancer Research and Treatment, 123(3), 819–828. doi: 10.1007/s10549-010-1088-4.PubMedCentralPubMedCrossRefGoogle Scholar
  46. 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(20), 2500–2508. doi: 10.1200/JCO.2011.38.5674.PubMedCrossRefGoogle Scholar
  47. McDonald, B. C., Conroy, S. K., Smith, D. J., West, J. D., & Saykin, A. J. (2013). Frontal gray matter reduction after breast cancer chemotherapy and association with executive symptoms: a replication and extension study. Brain, Behavior, and Immunity, 30(Suppl), S117–S125. doi: 10.1016/j.bbi.2012.05.007.PubMedCrossRefGoogle Scholar
  48. Myers, J. S. (2010). The possible role of cytokines in chemotherapy-induced cognitive deficits. Advances in Experimental Medicine and Biology, 678, 119–123.PubMedCrossRefGoogle Scholar
  49. Nelson, W. L., & Suls, J. (2013). New approaches to understand cognitive changes associated with chemotherapy for non-central nervous system tumors. Journal of Pain and Symptom Management, 46(5), 707–721. doi: 10.1016/j.jpainsymman.2012.11.005.PubMedCrossRefGoogle Scholar
  50. Pomykala, K. L., de Ruiter, M. B., Deprez, S., McDonald, B. C., & Silverman, D. H. (2013a). Integrating imaging findings in evaluating the post-chemotherapy brain. Brain Imaging and Behavior. doi: 10.1007/s11682-013-9239-y.Google Scholar
  51. Pomykala, K. L., Ganz, P. A., Bower, J. E., Kwan, L., Castellon, S. A., Mallam, S., et al. (2013b). The association between pro-inflammatory cytokines, regional cerebral metabolism, and cognitive complaints following adjuvant chemotherapy for breast cancer. Brain Imaging and Behavior. doi: 10.1007/s11682-013-9243-2.Google Scholar
  52. Risacher, S. L., Kim, S., Shen, L., Nho, K., Foroud, T., Green, R. C., et al. (2013). The role of apolipoprotein E (APOE) genotype in early mild cognitive impairment (E-MCI). Frontiers in Aging Neuroscience, 5, 11. doi: 10.3389/fnagi.2013.00011.PubMedCentralPubMedGoogle Scholar
  53. Saykin, A. J., Ahles, T. A., & McDonald, B. C. (2003). Mechanisms of chemotherapy-induced cognitive disorders: neuropsychological, pathophysiological, and neuroimaging perspectives. Seminars in Clinical Neuropsychiatry, 8(4), 201–216.PubMedGoogle Scholar
  54. Saykin, A. J., Shen, L., Foroud, T. M., Potkin, S. G., Swaminathan, S., Kim, S., et al. (2010). Alzheimer's Disease Neuroimaging Initiative biomarkers as quantitative phenotypes: Genetics core aims, progress, and plans. Alzheimers Dement, 6(3), 265–273. doi: 10.1016/j.jalz.2010.03.013.PubMedCentralPubMedCrossRefGoogle Scholar
  55. Scherling, C., Collins, B., Mackenzie, J., Bielajew, C., & Smith, A. (2011). Pre-chemotherapy differences in visuospatial working memory in breast cancer patients compared to controls: an FMRI study. Frontiers in Human Neuroscience, 5, 122. doi: 10.3389/fnhum.2011.00122.PubMedCentralPubMedCrossRefGoogle Scholar
  56. 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(5), 543–560. doi: 10.1080/13803395.2012.666227.PubMedCrossRefGoogle Scholar
  57. Seigers, R., Schagen, S. B., Van Tellingen, O., & Dietrich, J. (2013). Chemotherapy-related cognitive dysfunction: current animal studies and future directions. Brain Imaging Behav, 1–7. doi: 10.1007/s11682-013-9250-3
  58. Shen, L., Thompson, P. M., Potkin, S. G., Bertram, L., Farrer, L. A., Foroud, T. M., et al. (2013). Genetic analysis of quantitative phenotypes in AD and MCI: imaging, cognition and biomarkers. Brain Imaging and Behavior. doi: 10.1007/s11682-013-9262-z.Google Scholar
  59. 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 and Treatment, 103(3), 303–311. doi: 10.1007/s10549-006-9380-z.PubMedCrossRefGoogle Scholar
  60. Silverman, D. H., Mosconi, L., Ercoli, L., Chen, W., & Small, G. W. (2008). Positron emission tomography scans obtained for the evaluation of cognitive dysfunction. Seminars in Nuclear Medicine, 38(4), 251–261. doi: 10.1053/j.semnuclmed.2008.02.006.PubMedCrossRefGoogle Scholar
  61. Small, B. J., Rawson, K. S., Walsh, E., Jim, H. S., Hughes, T. F., Iser, L., et al. (2011). Catechol-O-methyltransferase genotype modulates cancer treatment-related cognitive deficits in breast cancer survivors. Cancer, 117(7), 1369–1376. doi: 10.1002/cncr.25685.PubMedCrossRefGoogle Scholar
  62. Sporns, O. (2013a). The human connectome: origins and challenges. NeuroImage, 80, 53–61. doi: 10.1016/j.neuroimage.2013.03.023.PubMedCrossRefGoogle Scholar
  63. Sporns, O. (2013b). Structure and function of complex brain networks. Dialogues in Clinical Neuroscience, 15(3), 247–262.PubMedCentralPubMedGoogle Scholar
  64. Sporns, O., Tononi, G., & Kotter, R. (2005). The human connectome: a structural description of the human brain. PLoS Computational Biology, 1(4), e42. doi: 10.1371/journal.pcbi.0010042.PubMedCentralPubMedCrossRefGoogle Scholar
  65. Stewart, A., Bielajew, C., Collins, B., Parkinson, M., & Tomiak, E. (2006). A meta-analysis of the neuropsychological effects of adjuvant chemotherapy treatment in women treated for breast cancer. Clinical Neuropsychology, 20(1), 76–89. doi: 10.1080/138540491005875.CrossRefGoogle Scholar
  66. 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(11), 2233–2239. doi: 10.1200/JCO.2004.08.094.PubMedCrossRefGoogle Scholar
  67. Versace, F., Engelmann, J. M., Jackson, E. F., Slapin, A., Cortese, K. M., Bevers, T. B. et al. (2013). Brain responses to erotic and other emotional stimuli in breast cancer survivors with and without distress about low sexual desire: a preliminary fMRI study. Brain Imaging Behav, 1–10. doi: 10.1007/s11682-013-9252-1
  68. Vodermaier, A. (2009). Breast cancer treatment and cognitive function: the current state of evidence, underlying mechanisms and potential treatments. Women's Health (London, England), 5(5), 503–516. doi: 10.2217/whe.09.36.CrossRefGoogle Scholar
  69. Walker, C. H., Drew, B. A., Antoon, J. W., Kalueff, A. V., & Beckman, B. S. (2012). Neurocognitive effects of chemotherapy and endocrine therapies in the treatment of breast cancer: recent perspectives. Cancer Investigation, 30(2), 135–148. doi: 10.3109/07357907.2011.636116.PubMedCrossRefGoogle Scholar
  70. 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(11), 2292–2299. doi: 10.1002/cncr.20272.PubMedCrossRefGoogle Scholar
  71. Wefel, J. S., Witgert, M. E., & Meyers, C. A. (2008). Neuropsychological sequelae of non-central nervous system cancer and cancer therapy. Neuropsychology Review, 18(2), 121–131. doi: 10.1007/s11065-008-9058-x.PubMedCrossRefGoogle Scholar
  72. Wefel, J. S., Vardy, J., Ahles, T., & Schagen, S. B. (2011). International Cognition and Cancer Task Force recommendations to harmonise studies of cognitive function in patients with cancer. Lancet Oncology, 12(7), 703–708. doi: 10.1016/S1470-2045(10)70294-1.PubMedCrossRefGoogle Scholar
  73. Weiner, M. W., Veitch, D. P., Aisen, P. S., Beckett, L. A., Cairns, N. J., Green, R. C., et al. (2013). The Alzheimer’s disease neuroimaging initiative: a review of papers published since its inception. Alzheimers Dement, 9(5), e111–e194. doi: 10.1016/j.jalz.2013.05.1769.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Andrew J. Saykin
    • 1
    Email author
  • Michiel B. de Ruiter
    • 2
    • 3
  • Brenna C. McDonald
    • 1
  • Sabine Deprez
    • 4
  • Daniel H. S. Silverman
    • 5
  1. 1.Center for Neuroimaging, Department of Radiology and Imaging Sciences and the Melvin and Bren Simon Cancer CenterIndiana University School of MedicineIndianapolisUSA
  2. 2.Department of Psychosocial Research and EpidemiologyNetherlands Cancer InstituteAmsterdamThe Netherlands
  3. 3.Department of Radiology, Academic Medical CenterUniversity of AmsterdamAmsterdamThe Netherlands
  4. 4.Radiology, University Hospital Leuven & Department of Imaging and PathologyKU LeuvenLeuvenBelgium
  5. 5.Ahmanson Translational Imaging Division, Department of Molecular & Medical Pharmacology, David Geffen School of MedicineUniversity of CaliforniaLos AngelesUSA

Personalised recommendations