Neurocognitive deficits after radiation therapy for brain malignancies

American Journal of Clinical Oncology: Cancer Clinical Trials

Volumn 38, Issue 6, 2015, Pages 634-640

  Saad, Shumaila ^a   Wang, Tony J C ^a  

^a New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

Brain tumors; Neurocognitive functions; Quality of life; Radiation therapy

Indexed keywords

ANTICONVULSIVE AGENT; CORTICOSTEROID; INDOMETACIN; MEMANTINE; NEUROTRANSMITTER; RAMIPRIL; REACTIVE OXYGEN METABOLITE;

AMNESIA; ANTICONVULSANT THERAPY; BLOOD BRAIN BARRIER; BRAIN TUMOR; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CANCER SURVIVAL; COGNITION; COGNITIVE DEFECT; DEMYELINATION; DISEASE DURATION; DISEASE SEVERITY; EXECUTIVE FUNCTION; GLIOBLASTOMA; GLIOMA; HUMAN; INFORMATION PROCESSING; INFORMATION RETRIEVAL; MENTAL HEALTH; NEUROANATOMY; OUTCOME ASSESSMENT; PRIMARY CENTRAL NERVOUS SYSTEM LYMPHOMA; QUALITY OF LIFE; RADIATION INJURY; RADIATION NECROSIS; REVIEW; SKULL IRRADIATION; SMALL CELL LUNG CANCER; SURVIVAL RATE; WHITE MATTER INJURY; BRAIN; BRAIN NEOPLASMS; BREAST TUMOR; COGNITION DISORDERS; FEMALE; LUNG TUMOR; LYMPHOMA; MALE; MELANOMA; NEUROCOGNITIVE DISORDERS; PATHOLOGY; PATHOPHYSIOLOGY; PSYCHOLOGY; SECONDARY;

BRAIN; BRAIN NEOPLASMS; BREAST NEOPLASMS; COGNITION DISORDERS; FEMALE; GLIOMA; HUMANS; LUNG NEOPLASMS; LYMPHOMA; MALE; MELANOMA; NEUROCOGNITIVE DISORDERS; RADIATION INJURIES;

EID: 84948567395     PISSN: 02773732     EISSN: 1537453X     Source Type: Journal    
DOI: 10.1097/COC.0000000000000158     Document Type: Review

References (97)

1. McDuff SG, Taich ZJ, Lawson JD, et al. Neurocognitive assessment following whole brain radiation therapy and radiosurgery for patients with cerebral metastases. J Neurol Neurosurg Psychiatry. 2013; 84: 1384-1391.
2. Sperduto PW, Chao ST, Sneed PK, et al. Diagnosis-specific prognostic factors, indexes, and treatment outcomes for patients with newly diagnosed brain metastases: a multi-institutional analysis of 4, 259 patients. Int J Radiat Oncol Biol Phys. 2010; 77: 655-661.
3. Zimm S, Wampler GL, Stablein D, et al. Intracerebral metastases in solid-tumor patients: natural history and results of treatment. Cancer. 1981; 48: 384-394.
4. Gaspar L, Scott C, Rotman M, et al. Recursive partitioning analysis (RPA) of prognostic factors in three Radiation Therapy Oncology Group (RTOG) brain metastases trials. Int J Radiat Oncol Biol Phys. 1997; 37: 745-751.
5. Tosoni A, Ermani M, Brandes AA. The pathogenesis and treatment of brain metastases: a comprehensive review. Crit Rev Oncol Hematol. 2004; 52: 199-215.
6. Abayomi OK. Pathogenesis of cognitive decline following therapeutic irradiation for head and neck tumors. Acta Oncol. 2002; 41: 346-351.
7. Butler JM, Rapp SR, Shaw EG. Managing the cognitive effects of brain tumor radiation therapy. Curr Treat Options Oncol. 2006; 7: 517-523.
8. Brown PD, Buckner JC, O'Fallon JR, et al. Importance of baseline mini-mental state examination as a prognostic factor for patients with low-grade glioma. Int J Radiat Oncol Biol Phys. 2004; 59: 117-125.
9. Taphoorn MJ, Klein M. Cognitive deficits in adult patients with brain tumours. Lancet Neurol. 2004; 3: 159-168.
10. Meyers CA, Smith JA, Bezjak A, et al. Neurocognitive function and progression in patients with brain metastases treated with whole-brain radiation and motexafin gadolinium: results of a randomized phase III trial. J Clin Oncol. 2004; 22: 157-165.
11. Ghia A, Tome WA, Thomas S, et al. Distribution of brain metastases in relation to the hippocampus: implications for neurocognitive functional preservation. Int J Radiat Oncol Biol Phys. 2007; 68: 971-977.
12. Mehta MP, Tsao MN, Whelan TJ, et al. The American Society for Therapeutic Radiology and Oncology (ASTRO) evidence-based review of the role of radiosurgery for brain metastases. Int J Radiat Oncol Biol Phys. 2005; 63: 37-46.
13. Schultheiss TE, Kun LE, Ang KK, et al. Radiation response of the central nervous system. Int J Radiat Oncol Biol Phys. 1995; 31: 1093-1112.
14. Chang EL, Akyurek S, Avalos T, et al. Evaluation of peritumoral edema in the delineation of radiotherapy clinical target volumes for glioblastoma. Int J Radiat Oncol Biol Phys. 2007; 68: 144-150.
15. Constine LS, Konski A, Ekholm S, et al. Adverse effects of brain irradiation correlated with MR and CT imaging. Int J Radiat Oncol Biol Phys. 1988; 15: 319-330.
16. Armstrong CL, Corn BW, Ruffer JE, et al. Radiotherapeutic effects on brain function: double dissociation of memory systems. Neuropsychiatry Neuropsychol Behav Neurol. 2000; 13: 101-111.
17. Meyers CA, Geara F, Wong PF, et al. Neurocognitive effects of therapeutic irradiation for base of skull tumors. Int J Radiat Oncol Biol Phys. 2000; 46: 51-55.
18. Moretti R, Torre P, Antonello RM, et al. Neuropsychological evaluation of late-onset post-radiotherapy encephalopathy: a comparison with vascular dementia. J Neurol Sci. 2005; 229-230: 195-200.
19. Schuz A, Preissl H. Basic connectivity of the cerebral cortex and some considerations on the corpus callosum. Neurosci Biobehav Rev. 1996; 20: 567-570.
20. Jokinen H, Ryberg C, Kalska H, et al. Corpus callosum atrophy is associated with mental slowing and executive deficits in subjects with age-related white matter hyperintensities: the LADIS Study. J Neurol Neurosurg Psychiatry. 2007; 78: 491-496.
21. Buckner RL. Functional-anatomic correlates of control processes in memory. J Neurosci. 2003; 23: 3999-4004.
22. Dobbins C, Russell EW. Left temporal lobe brain damage pattern on the Wechsler Adult Intelligence Scale. J Clin Psychol. 1990; 46: 863-868.
23. Izquierdo I, Medina JH. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem. 1997; 68: 285-316.
24. Raber J. Unintended effects of cranial irradiation on cognitive function. Toxicol Pathol. 2010; 38: 198-202.
25. Yazlovitskaya EM, Edwards E, Thotala D, et al. Lithium treatment prevents neurocognitive deficit resulting from cranial irradiation. Cancer Res. 2006; 66: 11179-11186.
26. Barani IJ, Benedict SH, Lin PS. Neural stem cells: implications for the conventional radiotherapy of central nervous system malignancies. Int J Radiat Oncol Biol Phys. 2007; 68: 324-333.
27. Cameron HA, Woolley CS, McEwen BS, et al. Differentiation of newly born neurons and glia in the dentate gyrus of the adult rat. Neuroscience. 1993; 56: 337-344.
28. Chakraborti A, Allen A, Allen B, et al. Cranial irradiation alters dendritic spine density and morphology in the hippocampus. PLoS One. 2012; 7: e40844.
29. Middleton FA, Strick PL. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev. 2000; 31: 236-250.
30. Berger A, Sadeh M, Tzur G, et al. Task switching after cerebellar damage. Neuropsychology. 2005; 19: 362-370.
31. Beauchamp MH, Dagher A, Aston JA, et al. Dynamic functional changes associated with cognitive skill learning of an adapted version of the Tower of London task. Neuroimage. 2003; 20: 1649-1660.
32. Hayter AL, Langdon DW, Ramnani N. Cerebellar contributions to working memory. Neuroimage. 2007; 36: 943-954.
33. Kirschen MP, Chen SH, Schraedley-Desmond P, et al. Load- and practice-dependent increases in cerebro-cerebellar activation in verbal working memory: an fMRI study. Neuroimage. 2005; 24: 462-472.
34. Ravizza SM, McCormick CA, Schlerf JE, et al. Cerebellar damage produces selective deficits in verbal working memory. Brain. 2006; 129: 306-320.
35. Meyers CA, Brown PD. Role and relevance of neurocognitive assessment in clinical trials of patients with CNS tumors. J Clin Oncol. 2006; 24: 1305-1309.
36. Correa DD, Maron L, Harder H, et al. Cognitive functions in primary central nervous system lymphoma: literature review and assessment guidelines. Ann Oncol. 2007; 18: 1145-1151.
37. Welzel G, Fleckenstein K, Mai SK, et al. Acute neurocognitive impairment during cranial radiation therapy in patients with intracranial tumors. Strahlenther Onkol. 2008; 184: 647-654.
38. Hopewell JW, van der Kogel AJ. Pathophysiological mechanisms leading to the development of late radiation-induced damage to the central nervous system. Front Radiat Ther Oncol. 1999; 33: 265-275.
39. Kamiryo T, Kassell NF, Thai QA, et al. Histological changes in the normal rat brain after gamma irradiation. Acta Neurochir (Wien). 1996; 138: 451-459.
40. Coderre JA, Morris GM, Micca PL, et al. Late effects of radiation on the central nervous system: role of vascular endothelial damage and glial stem cell survival. Radiat Res. 2006; 166: 495-503.
41. Alvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron. 2004; 41: 683-686.
42. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 1997; 17: 5046-5061.
43. Raber J, Rola R, LeFevour A, et al. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res. 2004; 162: 39-47.
44. Madsen TM, Kristjansen PE, Bolwig TG, et al. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience. 2003; 119: 635-642.
45. Fike JR, Rola R, Limoli CL. Radiation response of neural precursor cells. Neurosurg Clin N Am. 2007; 18: 115-127, x.
46. Mizumatsu S, Monje ML, Morhardt DR, et al. Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res. 2003; 63: 4021-4027.
47. Monje ML, Palmer T. Radiation injury and neurogenesis. Curr Opin Neurol. 2003; 16: 129-134.
48. Monje ML, Mizumatsu S, Fike JR, et al. Irradiation induces neural precursor-cell dysfunction. Nat Med. 2002; 8: 955-962.
49. Raju U, Gumin GJ, Tofilon PJ. Radiation-induced transcription factor activation in the rat cerebral cortex. Int J Radiat Biol. 2000; 76: 1045-1053.
50. Belka C, Budach W, Kortmann RD, et al. Radiation induced CNS toxicity-molecular and cellular mechanisms. Br J Cancer. 2001; 85: 1233-1239.
51. Logan A, Berry M. Transforming growth factor-beta 1 and basic fibroblast growth factor in the injured CNS. Trends Pharmacol Sci. 1993; 14: 337-342.
52. Chiang CS, Hong JH, Stalder A, et al. Delayed molecular responses to brain irradiation. Int J Radiat Biol. 1997; 72: 45-53.
53. Tsao MN, Li YQ, Lu G, et al. Upregulation of vascular endothelial growth factor is associated with radiation-induced blood-spinal cord barrier breakdown. J Neuropathol Exp Neurol. 1999; 58: 1051-1060.
54. Li YQ, Ballinger JR, Nordal RA, et al. Hypoxia in radiationinduced blood-spinal cord barrier breakdown. Cancer Res. 2001; 61: 3348-3354.
55. Lyubimova N, Hopewell JW. Experimental evidence to support the hypothesis that damage to vascular endothelium plays the primary role in the development of late radiation-induced CNS injury. Br J Radiol. 2004; 77: 488-492.
56. Hahn CA, Dunn RH, Logue PE, et al. Prospective study of neuropsychologic testing and quality-of-life assessment of adults with primary malignant brain tumors. Int J Radiat Oncol Biol Phys. 2003; 55: 992-999.
57. Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007; 114: 97-109.
58. Garside R, Pitt M, Anderson R, et al. The effectiveness and costeffectiveness of carmustine implants and temozolomide for the treatment of newly diagnosed high-grade glioma: a systematic review and economic evaluation. Health Technol Assess. 2007; 11: iii-iv, ix-221.
59. Meyers CA, Hess KR, Yung WK, et al. Cognitive function as a predictor of survival in patients with recurrent malignant glioma. J Clin Oncol. 2000; 18: 646-650.
60. Correa DD. Neurocognitive function in brain tumors. Curr Neurol Neurosci Rep. 2010; 10: 232-239.
61. Bosma I, Vos MJ, Heimans JJ, et al. The course of neurocognitive functioning in high-grade glioma patients. Neuro-oncol. 2007; 9: 53-62.
62. Corn BW, Wang M, Fox S, et al. Health related quality of life and cognitive status in patients with glioblastoma multiforme receiving escalating doses of conformal three dimensional radiation on RTOG 98-03. J Neurooncol. 2009; 95: 247-257.
63. Keime-Guibert F, Chinot O, Taillandier L, et al. Radiotherapy for glioblastoma in the elderly. N Engl J Med. 2007; 356: 1527-1535.
64. Taphoorn MJ, Schiphorst AK, Snoek FJ, et al. Cognitive functions and quality of life in patients with low-grade gliomas: the impact of radiotherapy. Ann Neurol. 1994; 36: 48-54.
65. Laack NN, Brown PD, Ivnik RJ, et al. Cognitive function after radiotherapy for supratentorial low-grade glioma: a North Central Cancer Treatment Group prospective study. Int J Radiat Oncol Biol Phys. 2005; 63: 1175-1183.
66. Torres IJ, Mundt AJ, Sweeney PJ, et al. A longitudinal neuropsychological study of partial brain radiation in adults with brain tumors. Neurology. 2003; 60: 1113-1118.
67. Douw L, Klein M, Fagel SS, et al. Cognitive and radiological effects of radiotherapy in patients with low-grade glioma: longterm follow-up. Lancet Neurol. 2009; 8: 810-818.
68. Correa DD, DeAngelis LM, Shi W, et al. Cognitive functions in low-grade gliomas: disease and treatment effects. J Neurooncol. 2007; 81: 175-184.
69. Correa DD, Shi W, Thaler HT, et al. Longitudinal cognitive follow-up in low grade gliomas. J Neurooncol. 2008; 86: 321-327.
70. Poortmans PM, Kluin-Nelemans HC, Haaxma-Reiche H, et al. High-dose methotrexate-based chemotherapy followed by consolidating radiotherapy in non-AIDS-related primary central nervous system lymphoma: European Organization for Research and Treatment of Cancer Lymphoma Group Phase II Trial 20962. J Clin Oncol. 2003; 21: 4483-4488.
71. Béhin A, Delattre J-Y. Neurologic sequelae of radiotherapy on the nervous system. In: Schiff D, Wen P, eds. Cancer Neurology in Clinical Practice. Totowa, NJ: Humana Press; 2003: 173-191.
72. Soussain C, Houillier C, Choquet S, et al. Primary CNS lymphoma-an update. Bull Cancer. 2014; 101: 314-324.
73. Correa DD, Shi W, Abrey LE, et al. Cognitive functions in primary CNS lymphoma after single or combined modality regimens. Neuro-oncol. 2012; 14: 101-108.
74. Harder H, Holtel H, Bromberg JE, et al. Cognitive status and quality of life after treatment for primary CNS lymphoma. Neurology. 2004; 62: 544-547.
75. Correa DD, Rocco-Donovan M, DeAngelis LM, et al. Prospective cognitive follow-up in primary CNS lymphoma patients treated with chemotherapy and reduced-dose radiotherapy. J Neurooncol. 2009; 91: 315-321.
76. Morris PG, Correa DD, Yahalom J, et al. Rituximab, methotrexate, procarbazine, and vincristine followed by consolidation reduceddose whole-brain radiotherapy and cytarabine in newly diagnosed primary CNS lymphoma: final results and long-term outcome. J Clin Oncol. 2013; 31: 3971-3979.
77. Laukkanen E, Klonoff H, Allan B, et al. The role of prophylactic brain irradiation in limited stage small cell lung cancer: clinical, neuropsychologic, and CT sequelae. Int J Radiat Oncol Biol Phys. 1988; 14: 1109-1117.
78. Herman MA, Tremont-Lukats I, Meyers CA, et al. Neurocognitive and functional assessment of patients with brain metastases: a pilot study. Am J Clin Oncol. 2003; 26: 273-279.
79. Welzel G, Fleckenstein K, Schaefer J, et al. Memory function before and after whole brain radiotherapy in patients with and without brain metastases. Int J Radiat Oncol Biol Phys. 2008; 72: 1311-1318.
80. Penitzka S, Steinvorth S, Sehlleier S, et al. Assessment of cognitive function after preventive and therapeutic whole brain irradiation using neuropsychological testing. Strahlenther Onkol. 2002; 178: 252-258.
81. Chang EL, Wefel JS, Hess KR, et al. Neurocognition in patients with brain metastases treated with radiosurgery or radiosurgery plus whole-brain irradiation: a randomised controlled trial. Lancet Oncol. 2009; 10: 1037-1044.
82. Aoyama H, Tago M, Kato N, et al. Neurocognitive function of patients with brain metastasis who received either whole brain radiotherapy plus stereotactic radiosurgery or radiosurgery alone. Int J Radiat Oncol Biol Phys. 2007; 68: 1388-1395.
83. Roos DE, Wirth A, Burmeister BH, et al. Whole brain irradiation following surgery or radiosurgery for solitary brain metastases: mature results of a prematurely closed randomized Trans-Tasman Radiation Oncology Group trial (TROG 98.05). Radiother Oncol. 2006; 80: 318-322.
84. Brown PD, Buckner JC, O'Fallon JR, et al. Effects of radiotherapy on cognitive function in patients with low-grade glioma measured by the folstein mini-mental state examination. J Clin Oncol. 2003; 21: 2519-2524.
85. Armstrong CL, Hunter JV, Ledakis GE, et al. Late cognitive and radiographic changes related to radiotherapy: initial prospective findings. Neurology. 2002; 59: 40-48.
86. O'Brien PC, Roos DE, Pratt G, et al. Combined-modality therapy for primary central nervous system lymphoma: long-term data from a phase II multicenter study (Trans-Tasman Radiation Oncology Group). Int J Radiat Oncol Biol Phys. 2006; 64: 408-413.
87. Abrey LE, DeAngelis LM, Yahalom J. Long-term survival in primary CNS lymphoma. J Clin Oncol. 1998; 16: 859-863.
88. Gondi V, Mehta MP, Pugh S, et al. Memory preservation with conformal avoidance of the hippocampus during whole-brain radiation therapy for patients with brain metastases: primary endpoint results of RTOG 0933. Int J Radiat Oncol Biol Phys. 2013; 87: 1186.
89. Gehring K, Sitskoorn MM, Gundy CM, et al. Cognitive rehabilitation in patients with gliomas: a randomized, controlled trial. J Clin Oncol. 2009; 27: 3712-3722.
90. Wefel JS, Kayl AE, Meyers CA. Neuropsychological dysfunction associated with cancer and cancer therapies: a conceptual review of an emerging target. Br J Cancer. 2004; 90: 1691-1696.
91. Chan AS, Cheung MC, Law SC, et al. Phase II study of alphatocopherol in improving the cognitive function of patients with temporal lobe radionecrosis. Cancer. 2004; 100: 398-404.
92. Shaw EG, Rosdhal R, D'Agostino RB Jr, et al. Phase II study of donepezil in irradiated brain tumor patients: effect on cognitive function, mood, and quality of life. J Clin Oncol. 2006; 24: 1415-1420.
93. Jenrow KA, Brown SL, Liu J, et al. Ramipril mitigates radiationinduced impairment of neurogenesis in the rat dentate gyrus. Radiat Oncol. 2010; 5: 6.
94. Jenrow KA, Brown SL, Lapanowski K, et al. Selective inhibition of microglia-mediated neuroinflammation mitigates radiationinduced cognitive impairment. Radiat Res. 2013; 179: 549-556.
95. Brown PD, Pugh S, Laack NN, et al. Memantine for the prevention of cognitive dysfunction in patients receiving whole-brain radiotherapy: a randomized, double-blind, placebo-controlled trial. Neuro-oncol. 2013; 15: 1429-1437.
96. Robbins ME, Zhao W, Garcia-Espinosa MA, et al. Reninangiotensin system blockers and modulation of radiation-induced brain injury. Curr Drug Targets. 2010; 11: 1413-1422.
97. Gondi V, Tome WA, Mehta MP. Why avoid the hippocampus? A comprehensive review. Radiother Oncol. 2010; 97: 370-376.